REVIEW | Energy & Environmental Science

Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics†
Peter J. le B. Williams* and Lieve M. L. Laurens‡
Received 26th November 2009, Accepted 18th February 2010 First published as an Advance Article on the web 22nd March 2010 DOI: 10.1039/b924978h Following scrutiny of present biofuels, algae are seriously considered as feedstocks for next-generation biofuels production. Their high productivity and the associated high lipid yields make them attractive options. In this review, we analyse a number aspects of large-scale lipid and overall algal biomass production from a biochemical and energetic standpoint. We illustrate that the maximum conversion efficiency of total solar energy into primary photosynthetic organic products falls in the region of 10%. Biomass biochemical composition further conditions this yield: 30 and 50% of the primary product mass is lost on producing cell protein and lipid. Obtained yields are one third to one tenth of the theoretical ones. Wasted energy from captured photons is a major loss term and a major challenge in maximising mass algal production. Using irradiance data and kinetic parameters derived from reported field studies, we produce a simple model of algal biomass production and its variation with latitude and lipid content. An economic analysis of algal biomass production considers a number of scenarios and the effect of changing individual parameters. Our main conclusions are that: (i) the biochemical composition of the biomass influences the economics, in particular, increased lipid content reduces other valuable compounds in the biomass; (ii) the ‘‘biofuel only’’ option is unlikely to be economically viable; and (iii) among the hardest problems in assessing the economics are the cost of the CO2 supply and uncertain nature of downstream processing. We conclude by considering the pressing research and development needs.

1. Introduction and historical background
1.1 History of biofuels development Without question our society will need to move away from its strong dependence upon fossil fuels as sources of energy and to

School of Ocean Sciences, University of Bangor, Menai Bridge, Anglesey, UK LL595PP † Electronic supplementary information (ESI) available: Appendices I–IV. See DOI: 10.1039/b924978h ‡ Current address: National Bioenergy Center, National Renewable Energy Laboratory, 1617 Cole Blvd, Golden, CO 80401, USA

reduce the emissions of greenhouse gases. Although alternatives exist for land-based transport – notably electrical power – there is an understandable reluctance to abandon liquid hydrocarbons and internal combustion engines for many transport purposes. Further, in the case of aviation transport and shipping, there is no practical alternative in the foreseeable future. These are amongst a number of reasons for the drive for the industrial development of liquid biofuels. Systems to produce biodiesel and bioethanol from crop plants (so-called firstgeneration biofuels) have been developed and optimised over the past several decades and are currently run as profitable businesses.

Broader context
There is a rapidly growing interest in the potential of microalgae as feedstocks for the next generation of biofuels. Working from fundamental biochemical principles, we consider the potential yields of organic production by photosynthesis. The maximum theoretical energy conversion of full spectrum sunlight to organic material lies in the region of 10%. The yields are constrained by thermodynamics and stoichiometry. The yields obtained with outdoor cultures are characteristically one third to one tenth of this theoretical yield; the losses are primarily due to the inability of the photosynthetic system to process the captured photons at the rate they are absorbed and so energy is lost. Overcoming this problem is a major challenge. The mass and, to a lesser extent, the energy yields are further reduced following the conversion of the primary photosynthetic products to the spectrum of biochemicals required by the cell. With a simple light-driven model, we explore the potential economics of a number of production scenarios of algae of varying lipid content (15–50% lipid of the cell’s dry weight) at low (0–30 ), intermediate (35–45 ) and high (45–55 ) latitudes. The main conclusions were that (i) the ‘‘fuel only’’ option is not viable, markets need to be found for the other major and minor components of the cell; (ii) high lipid containing algae may not necessarily be the most favourable candidate organisms. We conclude that although the potential does appear to exist for economic production of algal biofuels, a major R & D programme would be called for to convert the concept to a reality.
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Although the production and development of biodiesel and bioethanol has increased rapidly since the start of biofuels development and production in the 1970s, at 30–40% per annum, the total energy content in both biofuels is still less than 1% of the world’s energy production. The 2008 production figure for bioethanol was 2.5 Â 1018 joules and that for biodiesel an order of magnitude less by comparison to a total global energy use of 5 Â 1020 joules. Despite their relatively small contribution ($1%) to the overall production of liquid fuels, these first-generation biofuels have come under considerable international scrutiny and criticism. The main criticisms are the encroachment of the biofuels feedstock production on valuable crop and virgin land, and the effect biofuels have on food commodity prices. These issues have raised major question marks surrounding their social benefits, as summed up in the 2008 Gallagher report to UK House of Commons.129 The executive summary of that report noted that ‘‘feedstock production must avoid agricultural land that would otherwise be used for food production’’ and ‘‘The introduction of biofuels should be significantly slowed until adequate controls to address displacement effects are implemented and are demonstrated to be effective’’ (the embolding is ours). This mood, which although not universal, is widespread and has given rise to searches for alternative, so-called ‘‘second-generation’’ biofuels and has re-stimulated interest in mass algal biomass production. 1.2. Algal biofuels potential

We have restricted the review to microalgae. Macroalgae (seaweeds) have long been grown commercially and may have a role as biofuels and although a number of the aspects of their physiology are shared with the microalgae, their mass production involves a substantially different set of considerations. The advantages of microalgae as a feedstock for biodiesel production, over terrestrial plants, are that there is no requirement for soil fertility and, if marine algae are used, there is no need to draw upon valuable and often scare supplies of

freshwater. Thus, their negative ecological impact is much reduced as compared with higher plants.1 The potential to produce the feedstock on waste or desert land and the reduced freshwater requirements addresses some of the concerns in the Gallagher report. The mass production of microalgae for lipid production has a long history. Prior to the present interest in producing biofuels to mitigate CO2 release, there had been an extended period of research interest motivated by security of oil supply. This was initially prompted by the 1973 oil crisis. In response to the recognition of the potential vulnerability of oil supplies, Exxon Research and Engineering Company, for example, funded work of lipid production by algae.2 At about the same time (1978 to be precise), the U. S. Department of Energy set up the Aquatic Species Program (ASP). This program reached peak funding in the mid-1980s; after which the funding dwindled, until the program was eventually closed down in 1996. All told, just over $25 million was invested in the program. The findings, which were extensive and valuable, are collected in a major report.3 There was a concurrent Japanese programme, which purportedly cost in excess of $100 million, but which produced very little accessible science. The main conclusion of the ASP report was that algal biofuels are a potential valuable alternative to ‘traditional’ biofuels, however, considering the oil prices of the early 1990s, the calculated economics turned out to not be profitable. Nevertheless, considerable headway was made with regards to basic biology, strain selection, metabolic engineering and largescale growth cultures of selected strains. Algae have long been known to produce a great variety of lipids, hydrocarbons and other complex oils (reviewed recently in ref. 4,5). Cultured algae have been used as feeds for aquaculture applications because of their high content of nutritionally essential polyunsaturated fatty acids. A further motivation for algal culture has been the production of high value by-products such as the pigments astaxanthin (a food colorant and antioxidant from Haematococcus pluvialis) and b-carotene (a food additive produced from Dunaliella species). These sorts of

Peter Williams is professor emeritus at University of Bangor, UK. Originally trained as an industrial biochemist, he came to the view that oceanography offered more interesting challenges. He has held posts at the Woods Hole Oceanographic Institute, Southampton University, Bigelow Lab in Maine and the University of Gothenburg, returning to the UK to become Professor of Marine BiogeoPeter J: le B: Williams chemistry at Bangor University’s School of Ocean Sciences. His long term research interest has been the dynamics of organic material in the oceans, but an opportunity provided by Shell, opened up a new interest in the science behind algal biomass and biofuel production.
This journal is ª The Royal Society of Chemistry 2010

Dr Lieve Laurens is a researcher at the National Renewable Energy Laboratory (NREL) in Golden, Colorado. Prior to joining NREL, she was a Research Associate at the Centre for Applied Marine Science in the School of ocean Sciences, at the University of Bangor, UK, where she started research on biodiesel from microalgae and the work leading to this review was initiated. Her Lieve M: L: Laurens recent work focuses on the quantification and analysis of lipid yield and composition in microalgae using high-throughput spectroscopic methods. She holds a PhD from the Department of Metabolic Biology at the John Innes Centre in Norwich, UK.

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production processes have been in place since the early 1950s, so many aspects of the technology of mass algal growth may be considered mature.6 Much historical research has focused on the lipid composition from either a taxonomic or nutritional standpoint. There is, however, a sharp difference between the growth of algae for nutritional and for fuel use. These nutritional products are high value: astaxanthin for example commands a price in the region of $3 million tonneÀ1,7 compared with less than a $1000 tonneÀ1 for crude oil. Thus the economics are profoundly different. As a result, the production of biofuels will require a fundamental change in the approaches to production compared with nutraceutical and aquaculture feed-grade products and without question fresh, major challenges. Algal biomass can serve as a feedstock for the production of a variety of different biofuels, e.g. biodiesel, hydrogen, methane and bioethanol. Furthermore, its production is also being seriously considered for the removal of carbon dioxide from the flue gases of fossil fuel power stations. In order to maintain focus, we limit our discussion to the use of algae as feedstock for biodiesel and biomass production. There have been claims in the literature over recent years hailing algae as the solution to the global energy crisis (e.g. ref. 8). In this review we aim to present the principles behind large-scale production of algal biomass and biodiesel production along with a critical and objective review of the literature to date. As others (e.g. ref. 9), we build our review on the biochemical fundamentals of photosynthesis and biomass production, and accordingly begin (Section 2) with a brief discussion of the biology and biochemical composition of microalgae, with particular regard to the major biochemical categories: proteins, carbohydrates and lipids. In Section 3, starting from first principles, we establish the overall potential efficiency of photosynthetic production of algae. A major challenge in algal biofuels production is maximising this stage, as economic models for biodiesel production from seed oils have acknowledged that the feedstock cost comprises a substantial portion of the overall biodiesel cost.10 Accordingly, in Section 4 we address the growth of algae, the controls on growth and the reported yields. These are then combined with the theoretical photosynthetic yields to give predictions of biomass yields for season and latitude. Section 5 contains a review of the harvest and processing of the biomass relevant to published processes. In Section 6, we bring together the findings of the two preceding sections in the form of an economic analysis of various scenarios for low, mid and high latitudes. Finally, in Section 7, we explore the answers to two questions: (i) can the production of biofuels from algae be economically viable; and (ii) what R & D is needed to achieve a profitable outcome.

the eukaryotes and bacteria. They are able to photosynthesise, and are found in a range of different habitats, from fresh to marine and hyper-saline environments.11 The large number of species are generally subdivided into 10 taxonomic groups which include the green algae (Chlorophyceae), diatoms (Bacillariophyceae), yellow-green (Xanthophyceae), golden algae (Chrysophyceae), red algae (Rhodophyceae), brown algae (Phaeophyceae), dinoflagellates (Dinophyceae), Prasinophyceae and Eustigmatophyceae.12 The blue-green algae (Cyanophyceae) were originally grouped with the eukaryotic algae; however it was subsequently realised that they belong to the bacterial domain, hence their present common name – cyanobacteriax. A major and significant difference between the bacteria and the eukaryotes is that the former lack discrete internal, subcellular structures, organelles (chloroplasts, mitochondria, nuclei). Organelles are surrounded by lipid membranes whose bilayer structure requires strongly polar molecules. The triglycerides, the predominant lipid class in higher plant oils, lack the required polarity to form a sufficiently stable bilayer. The more polar phospholipids and the glycolipids are the major components of cell membranes and as a result, in actively growing cells, these two groups are major components of algal lipids, with important consequences. The metabolism of organisms, particularly microorganisms, is strongly influenced by their surface-to-volume ratio. Simple, single celled organisms can be approximated to spheres, thus their metabolism, and therefore growth rate, is inversely proportional to their cell diameters (see insert in Fig. 1). The growth rates of microorganisms can be very high; whilst some algae are able to divide once every 3–4 h, most divide every 1–2 days under favourable conditions (see Fig. 1). Accordingly their scope for growth is colossal and this, in major part, is the basis for the interest in their potential as biomass producers. In principle algal biomass crops may be harvested either daily or every few days (e.g. ref. 15, 16).


Major biochemical groups, their presence and function

It is conventional to consider four principal biochemical classes of molecules: carbohydrates, proteins, nucleic acids and lipids. Table 1 gives the broad cell content of these major fractions, their elemental composition and energetic properties. (i) Carbohydrates. Microorganisms contain a wide variety of carbohydrates, both monomers and polymers. Carbohydrates serve both structural and metabolic functions and, as the early products of photosynthesis, they serve as the starting point for the synthesis of the other biochemicals. Different classes of algae produce specific types of polysaccharides. For example, green algae produce starch as an energy store, consisting of both amylose and amylopectin, similar to higher plants. The green alga
x Strictly the term ‘‘alga’’ should be limited to the eukaryotic phototrophs, since cyanobacteria (formerly known as blue-green algae) are a form of bacteria, with very different genetics and evolutionary history. It is however very cumbersome to qualify every reference to these two groups of single-celled phototrophs as ‘‘algae and cyanobacteria’’, or as ‘‘micro-photoautotrophs’’ so, unless there is need to be specific, for convenience the two are referred in the text simply as ‘‘algae’’.

2. Biology and biochemical composition of microalgae
In this section we introduce the aspects of algal biology and biochemistry that are relevant in the economical considerations (Section 6). The composition of the algal biomass with regards to lipids, carbohydrates and proteins will greatly determine its overall value. Microalgae are single cell organisms, found in either colonies or individual cells and are comprised of representatives of both
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lipids serve both as energy reserves and structural components (membranes) of the cell.17N0.74N0. a linear polymer of b(1 / 3) and b(1 / 6) linked glucose units. A number of factors give rise to the variations seen in the table. Furthermore.83O0.1(i)) and also are embedded in the lipid membranes. P and S are the mass fractions of the constituent elements.22 Table 1 Elemental composition of algal biochemical components.21 Chrysolaminarin often accumulates in pyrenoids.3 Range of typical cell content (%) 15–60 — — — — — 20–60 3–5 10–50 This journal is ª The Royal Society of Chemistry 2010 Energy Environ. 2 shows the mean amino acid spectrum for a number of algae. using 18 kJ per mol of water as the energy lost on polymerisation. 3. As a consequence. The values for the lipid classes are derived from the mean fatty acid elemental composition and the composition of the other molecular structures in the overall molecule. which is the major site of the sulfur in algal lipids.2 33.11 Table 3 gives a summary of lipid class distribution derived from published analyses.1O + 6.40P0. Nucleic acids (RNA and DNA).83 Biochemical component Algal lipids Acylglycerides Glycolipids Phospholipids Algal fatty acid Methyl esters Protein Nucleic acid Polysaccharide Calculated calorific value/kJ gÀ1 36. Second.8 17.3 40.9 14.006 C1H1. 13 and algal growth-size relationships from ref.0035 C1H1. derived from data in ref. As with carbohydrates.83O0.17C + 116. Sci.3N0. The range given in the right hand column derives from the data compilations used to produce Fig. Allowing for the scatter due to differences in analytical techniques. 1 Frequency analysis of algal growth rates (main pane). Fig.4 35. 13.19 Red algae synthesise a carbohydrate polymer known as floridean starch. may gain a greater proportion of the overall lipid fraction as the metabolic rate slows down. It can be seen that the spectrum compares favourably with proteins of high nutritional quality. also the sites for photosynthetic activity in eukaryotes. the frequency distribution suggests a minimum cell lipid content in the region of 15% (see Fig.096 C1H1. 2010. shifts in lipid composition occur through the various phases of growth. For example. which are centres of high activity of carbon assimilation in the chloroplast.0014 C1H1. they provide the scaffold upon which the chlorophyll molecules are assembled in the light harvesting complexes of the chloroplast (see Section 3.024 C1H1. through the de novo synthesis and recycling of fatty acids to maintain the membrane characteristics.Proteins have important commodity value as animal feed.0031P0. for example.. 14. provide the basis for algal division and growth.12 C1H1.6 43. The microalgae have the facility for rapid adaptation to new environments (e.05 C1H1.18 This equation gives a good approximation for these compounds. accumulates 11 and 47% of its dry weight as starch in nutrient replete and deplete conditions respectively. see Section 3. The membrane lipids associated with the thylakoids (the internal chloroplast membranes. The values for the nucleic acids and carbohydrates are taken from ref.0 23. Storage lipids.3 39.91O0. which are predominantly triglycerides. 17. in conjunction with proteins and their monomers. That for the overall algal lipids is derived from the values for the individual lipid classes and the mean lipid class composition given in Table 3.56O0. Membranes are mainly constructed from phospholipids and glycolipids.g.23O0. 3 and 5. as well as a metabolic role.67O0. (iv) Lipids.47S. 5 (only the middle 90% of the data is used) Characteristic elemental composition C1H1. A large fraction of the cell’s phosphate may be present in phospholipids. The simple fatty acid triglycerides are important energy reserves. Critical to this is their amino acid composition. (iii) Nucleic acids. H.24S0. 3). There appears to be a marked difference between the total lipid content of the Fig. proteins also have both structural and metabolic functions. O. consisting mostly of amylose. Tetraselmis suecica. As do carbohydrates.11 C1H1. changes in temperature). As enzymes.012P0. they are the prime catalysts for cell metabolism and so facilitate growth. where they serve a similar structural role. The calorific values (as kJ gÀ1) of lipids and their derivatives have been calculated according to an equation for higher heating values (equivalent to the bomb calorific value) ¼ 35. (ii) Proteins. N.79O0.26S0.92O0. 554–590 | 557 .20 A commonly found polysaccharide in a large number of algal species is chrysolaminarin. Data for the proteins and fatty acids were derived from means from the analyses shown in Fig.006S0. they serve a structural role. The hydrogen and oxygen atoms associated with phosphate and sulfate were not included in the calculation.1(i)) contain a sulfur lipid (sulfoquinovosyldiacyl glycerol). where the hydrophilic polar phosphate or sugar moieties and the level of saturation of the fatty acyl chains determine the fluidity of the membranes.173N0. where C. as a number of amino acids are dietary essentials for mammals yet they are unable to synthesise them. The nucleic acids comprise a small fraction of cellular biomass but the major part of the cell’s phosphate and the second most important site of nitrogen (see Table 2). The calorific values for proteins and nucleic acids are calculated from the calorific values of their component molecules.25H À 11.88O0. it is known that the structural cell wall of Chlamydomonas reinhardtii consists primarily of cross-linked hydroxy-proline-rich glycoproteins.28N + 10.

A similar inverse relationship is also reported in ref. fuels with a higher level of unsaturation of the acyl chains have a higher cloud point. and ultimately in the resulting fuel. 6 contains data from two papers2. Overall production of lipid will be more complex than this simple analysis. 2.0014). from an economic point of view proteins are valuable bulk components of the cell (see Section 6). This journal is ª The Royal Society of Chemistry 2010 As the lipid content increases. e. Shifts in the biochemical composition with increasing lipid proteins preferentially run down or do the carbohydrates and proteins decrease in relative proportions. 3. 15% (from the analysis in ref. From these values. 42 data set is 0. The level of unsaturation affects biodiesel properties. To demonstrate the outcome. The product of the lipid content and growth rate will give a lipid-normalised production rate (in units of daysÀ1) and the relationship between this latter property and lipid content will take on a quadratic form. Sci. the question arises. 6 is general.. Furthermore. eukaryotic and the prokaryotic algae (the cyanobacteria) – the latter containing less than the former (see Fig. The fatty acid composition of algal lipids (Fig. As the lipid content increases. For two reasons the shift in protein content is critical. but are also much more susceptible to oxidation. 131. we might expect maintenance of growth rate with increases in lipid content up to 40–50%. The analysis gives a maximum lipid production rate at a lipid content of ca.3. 2). bespoke data sets are needed to establish to what extent the relationship seen in Fig. in designing a strategy to search and select for the economically most suitable algae. 5. These three trajectories are shown in the triangular plot in Fig. First these molecules set the level of the cell’s metabolism and in conjunction with the nucleic acids determine the growth rate potential. The highly unsaturated fatty acids found in algae may need to be hydrogenated to improve their potential fuel properties. The first derivative of the quadratic equation will give the lipid content for the maximum lipid production rate (mass of lipid produced per mass of lipid present in the culture per day). we have processed the parameters from the two equations given in Fig.23 The upper bars are the standard deviations. their potential as lipid producers would not appear to be promising. but the calculation brings home that high lipid content alone cannot regarded as the sole. Characteristic values for high quality proteins are shown for comparison purposes. 42’s data set) and ca. will be an important fuel quality determinant. 2 data set is 0. the lower the standard errors. with a high occurrence of unsaturated (and polyunsaturated) fatty acids. it is of prime importance to establish whether or not we can generalise over the change in protein content associated with changes in total lipid content. lipid and carbohydrate. So. consideration when searching for suitable strains or optimum growth conditions.1 (i)). are the carbohydrates preferentially run down and the protein content held constant as long as possible. Relationship between lipid content and growth and nutrient status Fig. 4) is well documented. 554–590 . 2 Mean amino acid composition of algal protein derived from 28 species (9 classes) of eukaryotic algae.g. however there is a significant inverse relationship between growth rate and lipid content (p value for ref.36 For example. Alternatively.2. In the case of first of the three scenarios listed above. Fig. with an intermediate maximum. whereas in the others we would anticipate a reduction in growth rate as the lipid content increased (see discussion below in Section 2. although the cyanobacteria are easier organisms to manipulate genetically (as a result of their simpler DNA). are the 558 | Energy Environ. an optimum growth rate for lipid metabolism may be calculated from the initial equation.42 and an analysis of the relationship between lipid content and growth rate. 5 gives a summary of the reported relative proportions of the three major biochemicals – protein. Second. the percentage of the sum of the other components must go down. 2. which is desirable. where their main function is to maintain membrane fluidity under different conditions. 5 does not give a clear sign of any systematic compositional trend and probably a dedicated study would be needed to elicit one. to allow culture dilution rates to be optimised without deleterious effect on overall lipid yield.0006 and that for ref. The majority of the unsaturated fatty acids occur in the membrane lipids. a high level of unsaturated fatty acids in a fuel increases the danger of polymerisation in the engine oil and can cause problems with oxidative stability of the fuel. However. The low value for tryptophan will derive in part from loss of the molecule during acid hydrolysis of the protein. The preponderance of the shorter chain fatty acids has significance for their potential as diesel fuels (defined as alkyl chains of between 12 and 18 carbon atoms long). of this procedure. likely to be due to the absence of internal membranes in the prokaryotes (see Section 2. 6. as there are many other considerations. Estimated maximum lipid production and growth rates are valuable for process design and management.Fig. The data we have been able to assemble in Fig. 2010. perhaps not even the major.3). 3). The high concentrations of unsaturated fatty acids in the extracted lipids. 30% (for ref. if it indeed exists. There is scatter in the data and the absolute rates differ. with half of the fatty acids having a carbon number less than C18. and potential. Thus.

The calculation is made using the elemental compositions and calorific values given in Table 1 and assumes that. These simplifications mean that the data are mainly illustrative Table 3 Mean (Æ standard error) lipid class content as a percent of total lipid of individual algal species. 554–590 | 559 High Biochemical composition (as % total mass) Medium This journal is ª The Royal Society of Chemistry 2010 Lipids 15 25 Proteins 48 42 Polysaccharides 32 28 Nucleic acids 5 5 Calorific value/kJ gÀ1 23.81 1. so one would expect these elements to be low to non-existent in algal biodiesel. the organisms were forced to terminate the production of nitrogen containing material (proteins and nucleic acids) but continued to synthesise lipids and carbohydrates. if present in fuels. the lipid class composition will also greatly affect the potential fuel yield by transesterification. Regardless of the biochemical mechanism. phosphorus and nitrogen-containing compounds would end up in the watersoluble fraction following transesterification. suggests that the matter may be more complex than ref.6 8. 5). 2010. the evidence for of a negative relationship between growth rate and lipid content (see Fig. 7). phosphorous and sulfur that may be problematic with regards to engine performance.g. as the lipid content varies.6 30 29 24 2. this provides an explanation for the apparent inverse relationship between growth rate and lipid content (see Fig.8 5. it cannot explain observations where growth was controlled by light rather than inorganic nitrogen and where again a negative relationship was seen. 43 suggested. Fig.42 This. 24). Thus triglycerides have a > 99% biodiesel yield compared to a < 70% Energy Environ. Whereas it may explain the lipid–nutrient relationship.4 36 64 0 0 Percentage major element in various biochemical fractions It has been known since the 1940s that cell lipid content increases during nutrient limitation (see Fig.4 0. Since about 30% of the original lipid mass can be lost to the polar phase during esterification. especially when products other than the lipid component are valuable (see e. Sci. However.7 P 0.1 0.5 20 49 27 3 C 53 . Algal oils differ from higher plant oils in their high phospholipid and glycolipid concentrations. 43 drew the broad conclusion that when the nitrogen ran out. we can anticipate a number of properties relevant to the potential of algal lipids to serve as fuels. 3. and other work. High Medium 33 24 36 7 14 32 48 6 8 34 52 6 63 22 13 2 36 39 23 2 23 47 28 3 59 24 13 3 33 41 23 3 Low O High Medium Low H High Lipid level Medium 55 60 7.. 6).4.Table 2 Calculated distribution of major elements in the four principal biochemical fractions for model low (15%).7 Element total (as % dry weight) Lipid level Low 50 27 18 5 28. plus a composite from all reports for microalgae. Ref. As nutrient limitation also affects growth rate.5 S 0 0. the nucleic acid content remains constant at 5% and protein : carbohydrate ratio remains constant at 3 : 2 (see legend to Fig.24–35 Simple lipids Diatoms Chaetoceros species Phaeodactylum tricornutum Range from Borowitzka (1988)130 Green algae Chlamydomonas species Dunaliella tertiolecta Dunalliella viridis Range from Borowitzka (1988)130 Blue green algae Range from Borowitzka (1988)130 Others Nannochloropsis oculata Isochrysis species Composite from all reports (n ¼ 46) 37 Æ 16 54 Æ 6 14–60 48 Æ 10 7Æ1 13 Æ 1 21–66 11–68 22 Æ 1 36 Æ 3 35 ± 3 Glycolipids 36 Æ 8 34 Æ 5 13–44 44 Æ 13 67 Æ 1 44 Æ 3 6–62 12–41 39 Æ 0 35 Æ 1 40 ± 2 Phospholipids 25 Æ 8 11 Æ 1 10–47 6Æ3 25 Æ 0 42 Æ 2 17–53 16–50 38 Æ 1 27 Æ 3 25 ± 2 High Medium 15 85 0 0 9 91 0 0 52 0 0 48 35 0 0 65 25 0 0 75 2 82 0 15 1 88 0 11 0 90 0 10 Low High Medium Low High Medium Low N 8. 6) has an important bearing on the strategy adopted for biomass production. Algal lipids as fuels Low From their molecular composition. These lipid classes contain nitrogen.2 24.7 7. it is likely that the sulfur. medium (25%) and high (50%) lipid-containing algae.2 7. A summary of the fuel properties of biodiesel from a microalga (heterotrophically grown Chlorella protothecoides)44 is given in Table 4.

Fig. their low calorific value would have no effect on the properties of the final biodiesel. 44. we do not place any great significance on the variance between these two sets of values. the chain length distribution of fatty acids occurring in microalgal species is more diverse compared with that of higher plants. 4 Upper histogram: mean fatty acid composition of various eukaryotic algal groups and Cyanobacteria. considering the two approaches used are so different. yield for phospholipids. This journal is ª The Royal Society of Chemistry 2010 . Full data set and references in Appendix III (provided in the ESI†). As shown in Fig. then the overall organic yield is reduced to ca. as these fractions would be almost certainly separated off in the transesterification process. Lower histogram: data for comparison purposes for higher plant fatty acids (C. Sci. Primary data and references in Appendix I (provided in the ESI†). as it could well be. From their calculated elemental composition (based on their reported fatty acid composition). if the methanol used is considered as part of the original organic supply.45 If the relative distribution of the lipid classes given in Table 3 is used. This figure does not take into consideration the consumption of methanol during esterification. The values in parentheses are the number of data sets used for the analysis. For example. slightly higher than 560 | Energy Environ. 2010. The upper error bars are standard deviations. we determine a heating value for the fatty acid methyl esters of 43 kJ gÀ1. 72%. strains that primarily accumulate shorter (<C16) chain fatty acids may be more amenable for use in the production of jet fuels. The figures in parenthesis are the numbers of analyses from which the means are derived. due to the lower calorific value of the glyco. 554–590 the figure of 41 kJ gÀ1 found in ref. 3 Frequency distribution of the lipid content (as % dry weight) of eukaryotic algae and Cyanobacteria. The difference is small and. The fuel characteristics will be greatly determined by the fatty acid composition and will thus vary with species and growth and nutrient conditions of the algal culture. then the overall mass yield on producing biodiesel is calculated to be about 80%. personal communication). compared to the application of very long chain fatty acids (>C20) in the lubricant market.. 4. This derives from a slightly higher value in our case for the C : H ratio (see Table 4). Shell Global Solutions. Price. the lower standard errors. Fig. 3. The overall heating value of crude algal lipid is somewhat depressed to a value in the region of 36 kJ gÀ1 (Table 1). making it possible that certain species will be cultured for selected fuel properties. However.and phospholipids.

Light reaction: 2H2O / 4[H] + O2 + energy Light-independent reactions: 4[H] + CO2 / [CH2O] + H2O (The notation [H] refers to the combination of the reduced coenzyme nicotinamide adenine dinucleotide phosphate (NADPH) and an electron. the red line that if the carbohydrate content diminishes as the lipid content increases and the magenta line that if the protein content diminishes. data taken from ref. Full data set and references in Appendix II (provided in the ESI†). The aim of this section is to provide a background to the theoretical and practical yield calculations in the subsequent sections so that the limitations to mass algal production can be made clear. 6 The variation of growth rate with lipid content. the above simple equation implies that at least 50% of the atoms of the oxygen produced must come from the carbon dioxide. carbohydrate 27. The data from ref. 2010. generating protons and oxygen. The upper error bar is the standard deviation. Photosynthesis is the predominant process maintaining a whole host of elements (notably carbon. Photosynthesis. whereas both derive from water. The data set from ref. 27 and 37–42. The red circle is the mean of the whole dataset for active growth (lipid 24. give rise to a charge separation and the ejection of electrons. 5 A: triangular plot of the proportions of lipid. which. it is also the ultimate source of all fossil fuels. The protons and the associated electrons enable the reduction of carbon dioxide to organic material.2%. The light reaction operates on very short time scales (from femtoseconds to milliseconds) whereas the { The notation [CH2O] is commonly used as shorthand for organic material in biology – in the present context its use is restricted to organic material with the same elemental ratio as monosaccharides. This journal is ª The Royal Society of Chemistry 2010 Energy Environ. protein 48. when absorbed by chlorophyll molecules. The values in parenthesis are number of observations from which the mean was derived. often referred to as ‘‘dark reactions’’ but better as ‘‘light-independent reactions’’. 7 The effect of nitrogen limitation on the lipid content of eukaryotic algae. protein and carbohydrate content of algae. 3. thus the more appropriate equation is: 2H2O + CO2 / [CH2O] + O2 + H2O This overall reaction can be separated into two phases: (i) a set of photochemical and redox reactions (conventionally called the ‘‘light reaction’’) and ii) a sequence of enzymatic reactions. These electrons are driving the dissociation of water. maintaining the biosphere. The green line shows the trajectory on increasing lipid composition assuming the protein : carbohydrate ratio remains constant.Fig. whereby oxygen is essentially a waste product. Fig.) These reactions + O2 + energy are intimately connected within the cell. in turn. Fig. the lower the standard error. Mechanism of photosynthesis The simple stoichiometry of photosynthesis may be written as: H2O + CO2 / [CH2O]{ + O2 However.1. 2 derives from 15 strains of freshwater and 11 strains of marine eukaryotic algae. Sci. The solid circles show the shift in composition from unlimited logarithmic growth (red) to N-limited growth (brown). 3. 42 comes from 8 eukaryotic marine algae commonly used in aquaculture.. Principles and efficiency of photosynthesis Since the basis of algal biomass production is directly proportional to the efficiency with which the algal cells assimilate carbon from the atmosphere through photosynthesis. nitrogen and sulfur) out of thermodynamic equilibrium. as they occur both in the light and the dark. the data used were taken during active logarithmic growth.3%. 3. In this case growth rate was controlled by varying the irradiance and the cultures were sampled during active growth. It is the basis of the food supply for most life on Earth. is driven by photons. 2. 554–590 | 561 .5%). we discuss the basic principles and efficiency of photosynthesis in this section. and thereby driving their global geochemical cycles. Throughout this review we have used a rounded off value of 3 : 2 for the protein carbohydrate ratio.

86–0.9] Higher plant 0. Fig.5–5.8 ASTM biodiesel standard 0. 0.Table 4 Comparison of properties of biodiesel from microalgae and diesel fuel and the ASTM biodiesel standard.5 40–45 1. 8 The distribution of energy (blue line) and photons flux (red line) in incoming radiation. The data from ref.5 — — light-independent reaction operates over timespans of seconds to hours. Algae can change the quantity of these accessory pigments (subject to phylogenetic constraints) to optimise light capture.374 41 [43] 1. Thus. 8. 9). There are small differences between their observations and the values we calculate (given in square parentheses) from elemental composition and calorific values given in Table 1 Properties Density/kg dmÀ3 Viscosity/mm2 sÀ1@ 40  C Flash point/ C Solidifying point/ C Filter plugging point/ C Acid value/mg KOH gÀ1 Heating value/kJ gÀ1 H/C ratio Micro-algal 0.16–0.838 1. but the adaptation process is slow compared with the time scales of the photochemical reactions. there is a net loss of some 21% of the original energy. 0.47 Since we use clear sky radiation as the Fig.3 Diesel fuel 0. The irradiance spectrum is shown in Fig. this is illustrated in Fig. Redrawn with permission from ref.877–0.864 5.1 75 –50–10 À3. This delimits the useful range of incoming radiation to 400–700 nm – so called photosynthetically active radiation (PAR). 8.43 39. However. its absorption and the formation of ‘‘reducing capacity’’. Sci. 9). 9 The spectrum of incoming radiation (black line) and the absorption spectrum of chlorophyll and accessory photosynthetic pigments. The primary pigment involved in photosynthesis is chlorophyll a. there is an inevitable loss of energy resulting from the transfer from high-energy. PAR amounts to 45–50% of the total incoming radiation. À6. The energy of photons. basis for further discussion here. 46. shorter wavelength to lower energy.7) Max.2 115 À12 À11 0. captured at shorter wavelengths. Plants have overcome this by introducing additional light capturing pigments (e. This journal is ª The Royal Society of Chemistry 2010 562 | Energy Environ.. the spectrum of light arriving at the surface of the planet has been attenuated by some 30% by the gases in the atmosphere and losses due to light scattering and absorption by clouds. photons.2 — — — 0. 9) so increasing the portion of the spectrum that can be used for photosynthesis.0 Min. This profound mismatch of timescales gives rise to inefficiencies in fluctuating environmental circumstances. can be transferred to the 680–700 nm region very efficiently on a quantum basis. < À 15 Max. (i) Light. b-carotene) that fill in much of the chlorophyll a window of the spectrum (see Fig. 44 comes from a heterotrophically grown Chlorella protothecoides culture.g. the 45% end of the spread is the more appropriate value to adopt.0 (max. 2010. The solar spectrum is described by Planck’s radiation distribution equation. longer wavelength. the exact value mainly being determined by the moisture content of the atmosphere attenuating the infrared part of the spectrum.9–4. Because of its low absorption in the range 450–650 nm. 3. notably irradiance and temperature variations and is a major problem in maximising yields of mass algal culture.5–40. chlorophyll a itself only is able to capture some 30–40% of PAR. 554–590 .8 [1. 0 Winter max. which has strong absorption bands in the regions 400–450 and 650–700 nm (see Fig.90 3.3–5. The photosynthetically active parts of the chlorophyll spectrum lie at 680 and 700 nm (see Fig. although the resultant quantum efficiency may be more or less constant throughout the PAR spectrum. 100 — Summer max. Not all incoming radiation is available for photosynthesis. The lower green line shows the residual energy after it has been transferred to a frequency equivalent to that of chlorophyll a at 680–700 nm absorption bands.887 3.

photosystem I (PSI). Briefly.Fig. and the statistical probability of arrival of 8 photons at a single k An einstein is defined as a mole of photons. Present consensus favours the latter. the protons spin a molecular rotor. charge separation.. 50 kJ molÀ1 ATP. l ¼ 680 nm) there is a charge separation of 1. This sets up a charge gradient. 3. The functioning of the water splitting system is described in detail in ref. known as thylakoids. The broad mechanism of the conversion of the photochemical energy into metabolic energy and reducing capability is complex. 48. 554–590 | 563 . with a free energy gain of ca. Some of the intermediates in the system have a limited lifespan. the total potential energy yield is 590 kJ per 4 moles electrons transported. ferredoxinNADP reductase (FNR) (in order of electron transport chain) and ATP synthase. 56). At the same time protons are pumped across the membrane into the inner cavity of the thylakoid (the lumen). generation of metabolic energy and reducing capability.** which gives rise to the synthesis of adenosine triphosphate (ATP). Although in theory this could be supplied by four photons (two einsteins at 680 nm and two at 700 nm would yield 692 kJ). of unprescribed wavelength. ‡‡ There have been two schools of thought over the number of photons required per molecule of O2 split: either 3–6 photons or 8–10 photons (see ref. there are two functionally separate sites of photon absorption. †† Depending upon the circumstances the DG for the hydrolysis of ATP varies from À45 to À55 kJ molÀ1.7 V and 1. The electron flow away from the chlorophyll molecules draws electrons from water. plastocyanin (PC). cytochrome b6f complex (Cyt b6f). producing a molecule of oxygen plus four protons. refer to the reaction centres of photosystem II (PSII) and I (PSI) respectively. The electrons pumped by the two reaction centres eventually give rise to the production of the reducing agent (NADPH) used in the process of carbon assimilation. Whereas the formation of electrons operates on a one-photon-per-electron basis. This journal is ª The Royal Society of Chemistry 2010 Energy Environ. at photosystem II (PSII. This whole complex of photon capturing mechanisms. although comparatively well understood. The photon absorption elicits a charge separation of at two reaction sites. the biological energy currency. plastoquinone (PQ). A mean figure of À50 kJ molÀ1 is used in the present account. Two molecules of NADPH are being produced per four electrons transported with a free energy gain of 220 kJ molÀ1 NADPH. photosystem II (PSII). The major functional units are represented as oval shapes. three ATP molecules are formed per 12 protons transported. 10 as the so-called ‘‘Z-scheme’’ of photosynthesis. ** It has been held that Nature never evolved a wheel – it however did a billion or more years ago and on the nanoscale! Only recently have we developed the skills to observe these molecular mechanisms.†† along with the two NADPH molecules. the asterisk (*) indicates the excited state. ferredoxin (Fd). l ¼ 700 nm) requiring respectively 164 and 154 kJ per einstein. being oxidised stepwise at four stages. The inset shows a schematic close-up of the light harvesting complex (LHC). P680 and P700.k This is depicted in Fig. In total. 2010. Sci. 10 Illustration of the light reactions of photosynthesis (the so-called Z-scheme). the fully oxidised form then draws the four electrons from two molecules of water in one step. On their return. the dissociation of water requires an accumulation of four electrons to effect the production of one molecule of oxygen. experimental observations suggest 8–10 photons‡‡ are needed per four electrons transported.6 V at photosystem I (PSI. and the water splitting system is embedded in the lipid membrane of flattened sac-like structures present in the chloroplast. A tetra-manganese complex acts as an accumulator. coupled in tandem by a chain of redox carrier molecules.

3. In addition. RuBisCO: ribulose bisphosphate carboxylase/oxygenase. RuBP: ribulose-1. Which reaction predominates depends upon the ratio of the partial pressures of the two gases. it has the curious property of catalysing both the carboxylation and oxidation of its substrate.phosphoglycerate. Most. however. The biochemistry is complex50 and incurs further demands on energy and. It has long been a puzzle why an enzyme. 10À10 s. (i) CO2 fixation. The ‘‘reducing power’’ (NADPH + H+) and energy (ATP) produced by the light reaction is used in the enzymatic ‘‘light-independent’’ part of photosynthesis to enable the incorporation of CO2 into organic material and its subsequent reduction (see Fig. G6P: glucose-6-phosphate. proteins etc. it accounts for a major fraction of all living protein. fatty acids. 12). Nature has overcome this problem by linking together approximately 2000 chlorophyll molecules in a light harvesting complex (LHC) with a much smaller number of reaction centre chlorophyll molecules. This reduction step is where the reducing power generated during the photochemical reactions is used. Carboxylation of Ru5BP in the Calvin cycle leads to the production of two molecules of 3-phosphoglyceric acid (3-PGA). These set of three carbon compounds are the building blocks for the synthesis of the basic biochemical fractions (see insert in Fig. that the enzyme is nearly perfectly optimised49 and that the perceived inefficiency is a fallacy. The necessary energy (ATP) and reductant (NADPH+ + H+) (not shown stoichiometrically) are originating from the photosynthetic light reactions. loss of carbon and oxygen. The first stable products of the reaction are 3-carbon organic acids. has seemingly remained so inefficient since there have been a billion or more years for improvements to have evolved. A simplified analysis is made in Box 1 for triglycerides and proteins based on hexoses as the starting point. G3P: glyceraldehyde-3-phosphate. The calorific value of the product is around 469 kJ molÀ1 C. the cells ultimately produce biomass which comprises lipids as well as proteins. RuBisCO exists as large heteromultimeric protein complex (536 kDa) and is an outstandingly sluggish catalyst. The captured energy of photons very rapidly passes through this network of chlorophyll molecules. This is termed the photosynthetic unit (see inset in Fig.5bisphosphate. On average there are about 300 chlorophyll molecules per active reaction centre. The average cycling time of one ‘round’ of CO2 assimilation is 100 to 500 ms. aquatic microalgae overcome the predominance of oxygen over carbon dioxide in oceans (ca. CO2 and O2. sugars.3 bis. It appears. and therefore biomass. Two matters are important to note here: first high lipid content is achieved at a cost of biomass loss. Fig. 12 shows the biomass loss with increase in lipid production. 30-fold) by actively pumping in CO2 and so increasing its concentration around RuBisCO.3-bisphosphoglycerate (1.3-BPGA: 1. 11 Schematic simplified representation of the Calvin-Benson cycle in three parts. 2010. 3-PGA: 3-phosphoglycerate. 564 | Energy Environ. RuBisCO plays a central role in all plant photosynthesis. 1. PEP: phosphoenolpyruvate. 10).. 554–590 This journal is ª The Royal Society of Chemistry 2010 . 11). 11). (ii) reduction and (iii) regeneration. but not all. where acetyl-CoA in an intermediate (lipids and some amino acids). The oxidation reaction is wasteful of energy. as carbon dioxide. 11). Fig. this results in something in the region of a 30–50% loss of the original photosynthetically produced organic material (see Fig. second. (ii) The ‘‘light-independent’’ reactions. which is subsequently phosphorylated to 1. reaching the reaction centre within a timescale of ca. Sci. It is from these compounds that all major biochemicals (fats. The first committed step is the carboxylation of the sugar ribulose 1 : 5 bisphosphate (Ru5BP) by the enzyme ribulose bisphosphate carboxylase oxygenase (RuBisCO). fixing 2–10 molecules of CO2 per active site per second.3-BPGA) and reduced to glyceraldehyde-3-phosphate (G3P). whereas ‘‘theoretical’’ calculations of photosynthetic efficiency are based on hexose production. of such crucial importance to life on Earth. F6P: fructose-6-phosphate.capturing site within the required time frame is low.) are eventually formed (see Fig.

Thus. 3. which must come from respiration. The elemental composition of algal protein may be calculated from the amino acid analysis as C1H1. and therefore additional mass. which incurs a considerable reduction in entropy. Y is the biomass yield in mass per mass hexose synthesised. reflecting the scales of the metabolic work needed. is estimated to be 120 kJ per peptide bond. If it is assumed that the protein to carbohydrate ratio is 3 : 2 and that this ratio remains constant with increase in lipid content. If there is a negative energy balance. to conserve energy there must be a mass loss of about 2. there is a small energy gain in the form of an ATP and two NAD(P)H. The overall synthesis of the primary lipid product – palmitic acid – from glucose may be divided into two phases: (i) the formation of acetyl CoA and (ii) and the conversion of acetyl CoA to palmitic acid.6L) (4) where C is the carbohydrate content (assuming it to be a hexose-based polysaccharide). If we take the mean figures for the proportions of these components of algal lipid given in Table 3.65 g gÀ1 protein.11C + 1.5. Note: C + P + L ¼ 1. however there will be the loss of 3ATP molecules for the formation of the triglyceride and additional losses when palmitic acid is desaturated to form other fatty acids. thus we may take a round figure of 1. Calculating the mass yields: given the values calculated above. rather than the hexose sugars are considered to be the starting point for lipid biosynthesis. and (ii) on their conversion to proteins (ref. 6%) of the overall calorific value of the protein. Note: NAD(P)H is used to refer to both NADH and NADPH. 10 000 kJ molÀ1) and can be largely ignored.7 g for the mass of hexose requires to synthesise 1 g of protein. the conversion of 4 molecules of a hexose to 1 mole of palmitic acid results in a drop in calorific value from 11 446 to 10 117 kJ.46 The energy required per gram of protein synthesised can be estimated from the nitrogen content of the protein and is small fraction (1. Thus. there is a substantial (2. much less than the formation of lipid. Algal lipid contains a substantial amount of phospholipid and glycolipid. is a minimum calculation. assuming no respiration of carbon. Nucleic acid synthesis: The calculation for the nucleic acids is extremely complex and. where FW is the formula weight (with carbon set as 1) and 30 is the formula weight of CH2O.9-fold) loss of mass. The energy for the second reaction. The mass loss in making phospholipid may be estimated to be about 2. The energy gain on a mass basis is much the same as the mass loss (1. there will also be metabolic work at two stages: (i) during the synthesis of the individual amino acids. then as well as the mass losses during the biochemical transformations the production of CO2 (see equation below). 4C6H12O6 / 8 acetyl CoA + 8CO2 + 8ATP + 16 NAD(P)H 8 acetyl CoA + 7ATP + 14 NAD(P)H / CH3(CH2)14COOH Overall: 4C6H12O6 / CH3(CH2)14COOH + 8CO2 + ATP + 2NAD(P)H (3) (1) (2) Thus. 2010. This can be estimated from the biochemical stoichiometry of the various reactions during the transformation of hexoses into lipids. the loss of mass on production protein from a hexose.. these calculations imply that. then the hexose mass required for its synthesis may be simply calculated as 30 Â PQ/FW (g gÀ1). For lipid. the general equation for the biomass yield is Y¼ 1/(1. in the case of protein by about 15%. These energy gains and losses are small (100–200 kJ per palmitic acid molecule) as compared with the overall energy present in the molecule (ca. a weighted mean value of 2.33) on a carbon basis. There will be a small energy gain if the triose phosphates. loss. is 1.3 – these values are not as certain as the triglyceride figure.4 kJ gÀ1. This journal is ª The Royal Society of Chemistry 2010 Energy Environ.46 + 1. Protein synthesis: The parallel calculation for the conversion of the photosynthetic products to proteins is more complex.7P + 2. Sci.56O0.Box 1: Biomass and energy losses incurred during the biosynthesis of lipids and proteins Lipid synthesis: The biosynthesis of high calorific value compounds such as lipids from the primary products of photosynthesis – hexoses – must incur a metabolic penalty in the form of loss of mass. However. This.7 kJ gÀ1 (a hexose) to 36 kJ gÀ1 (a generic algal lipid). 125 and personal communication) makes a very comprehensive analysis of the mass yield of synthesising the amino acids for protein synthesis and obtains a value of 1. whereas there is a small loss of energy (ca. 554–590 | 565 .6-fold loss of mass is obtained for algal lipid formation from hexose. 10%). Overall. then the equation simplifies to: Y ¼ 1/(1. it underestimates the demand 9%.e. the calculation has not been made. this has been used for the calculation of the mass yield of cells with varying lipid content. as the 2nd law of thermodynamics calls for some energy.7 and making glycolipid 2.14L) (5) Estimating mass loss from calculated the photosynthetic quotient (PQ): If there is little metabolic work involved in the conversion of photosynthetically produced hexose to another biochemical category. additional mass will be lost to provide the extra energy. A simple minimum calculation may be made from the change in calorific value from 15. however.36-fold. i.30N0. P is the protein content and L the lipid content. in view of their relatively small contribution to the overall mass of the cell.26S0.006 (see Table 1).

ref. There are thought to be differences between taxonomic groupings of algae (see Fig. 55. respirationassociated losses in terrestrial crop plants fall in the range of 30– 60%. 13A). B: Analysis of data obtained from cultures of algae in ref. In the case of microalgae. This journal is ª The Royal Society of Chemistry 2010 . This is a major limitation to achieving maximum photosynthetic efficiency in other than ideal laboratory situations. the dominant loss term is the photosynthetically associated respiration and the fraction of photosynthesis lost to concurrent respiration lies in the range 8–12%. and (ii) the mismatch of time scales between the light-dependent and independent reactions in photosynthesis can give rise to ‘‘traffic jams’’ along the electron transport chain when the former reaction gets ahead of the latter. There are a number of reasons. there is excess enzymatic activity. other than at very low rates of photosynthesis. In the near-linear initial part of the curve. which probably represents some basic maintenance energy.53 Normally. 3. The flattening off of the curve at higher irradiances is a consequence of the limitation of the rate of photosynthesis by Fig.4(ii) and Box 2). Shown also is the hexose energy required to synthesise biomass of varying lipid content. the penalty is wastage of the energy from the captured photons. By contrast respiration is more complex.2 Respiration At first it may seem surprising that plants. The compensation irradiance takes on importance in dense algal cultures (see Section 4.46 MJ mÀ2 dÀ1 of incoming solar radiation). Photosynthesis can in most part be treated as one of two alternative pathways.01 to 0. and (ii) a photosynthetically-associated component. As respiration continues in the dark. 12 Graph of the calculated yields of biomass (green line) from hexose for biomass with varying lipid contents. this assumption has a minor effect on the outcome of the calculations.3 Overall efficiency of photosynthesis The energetics of the photochemical reactions in photosynthesis and the linked enzymatic reactions associated with carbon assimilation have been covered above. The 566 | Energy Environ. which may result from the above decongestion process but also from repair or replacement of the components of the light gathering system which suffer photo-damage. Sci. with light limiting the photosynthetic rate. 3. Gonyaulax tamarensis. 53 suggests that the major part of the variation can be attributed to individual cell biomass: Ec is approximately proportional to the square root of cell mass. 3. reported values show a wide range from 03 to 12 mE mÀ2 sÀ1 PAR (equivalent to 0. By comparison. We now consider the relationship between the photon flux (the irradiance) and the resultant photosynthetic rate. A careful analysis of these two forms of respiration for the major algae groupings has been made. 13B) and ref. 14). The hexose is assumed to have a calorific value of 15. The analysis in ref. 53. 51 list four other forms of respiration in plants. should need a supplementary energy generating process.. which illustrates the offset due to the compensation irradiance. overall respiration can be treated operationally as a composite of two components: (i) a biomassassociated component. In addition to the widespread so-called ‘‘mitochondrial respiration’’. 13 A: Schematic of the various components of respiration and their effect on net metabolism. Box 1. 554–590 Fig. and maximum quantum yields are obtained. However. The protein : polysaccharide ratio is taken to be constant at 3 : 2.54 The point at which the respiration and photosynthesis curves intersect is the ‘‘compensation point’’ and the irradiance at this level is known as the compensation irradiance (Ec). The calculation is based on eqn (5). so plants need some energy generating process independent of light. the two main ones being: (i) to sustain their metabolism over periods of darkness. a large dinoflagellate. Net growth only occurs at light levels above this value. that have the ability to create metabolic energy de novo.7 kJ gÀ1.compensation irradiance is seen as an offset on the photosynthesis–irradiance curve (see Fig. these numbers are roughly twice as great over a 24 h diel cycle. Respirationlike electron disposing reactions have evolved to alleviate this congestion. would not be a candidate organism for mass algal culture but is included as the compensation irradiance is clearly shown with this organism. 2010. Characteristically the relationship is nonlinear (see Fig.

6 V (PSI) (equivalent to 1267 kJ in total) imply very efficient energy transfer at this stage. This would give a range for Emin from 0. The latter is Fig. the 24 h compensation irradiance. Thus. 52. with a geometric mean of 0. 3. 54. A quantum yield of 10 would give rise to a proportionately lower yield. 56.3 MJ mÀ2 dÀ1 (see ref. the main light absorbing pigment. It would appear that the low light adapted form is the default state. such that the photosynthetic system saturates at higher irradiances.e. growth will only occur when the daily average irradiance (E) through the culture is greater than the compensation irradiance (Ec) i. based on total incoming radiation.127 Assuming the distribution of light with depth complies with Beer’s law.Box 2: Estimating the light threshold for growth of dense algal cultures In dense. well-mixed algal cultures. eqn (4) reduces to: Emin ¼ 7. If the high irradiances are sustained for an hour or so. has a wide scatter. the light extinction coefficient will be in the region of 50 mÀ1. In dense cultures eÀkz(1. and the hatched area between this and the blue curved line for photosynthesis is an indication of the photon wastage. The minimum incoming irradiance level that will allow growth (Emin) may be calculated 0 according to Sverdrup’s critical depth theory. 2010. In this zone. It is in the context of this effect that the time scale mismatch of the photochemical and enzymatic parts of photosynthesis becomes significant. either by fluorescence or by one of the respiratory decongesting mechanisms.. The dashed black line is a projection of the initial rate. to be 2% of the cell dry weight and to have a specific light attenuation of 10 m2 gÀ1 (derived from data in ref. then the algae will adapt to them.03 to 0.5Ec 0 (5) For candidate algae.25 kg dry weight mÀ3. 0 enzymatic reactions. by either increasing their enzymatic capacity but more commonly by reducing the capturing efficiency of photons. It is important to stress that the following calculation of the efficiency of photosynthesis restricts its attention to the ideal circumstance. Thus. for a raceway 15 cm deep. then the above integral with depth has the following solution Pz 0E ¼ (E0/k)(1ÀeÀkz) (2) where k is the beam attenuation coefficient (extinction coefficient).7 V (PSII) and 1. (E)/z $ Ec (1) where z is the depth of the culture. The phenomenon of light adaptation has a major influence on the yields of optically dense cultures as will be discussed in a later section. Sci. 53 and 55).2 to 2 MJ mÀ2 dÀ1. the algae can exist as two physiological types – low light adapted (high chlorophyll content) and high light adapted (low chlorophyll content).12 MJ mÀ2 dÀ1. The consequential voltage jumps of 1. Even under these circumstances it is not a straightforward calculation and all too often the complications are overlooked or bypassed. The present calculation is made for the production of one mol of organic carbon (of a formula CH2O). 14 The photosynthesis versus irradiance (PvE) relationship. This assumes chlorophyll. this lowers the slope of the initial part of the curve. assumed to have a heat of combustion of 469 kJ mo1À1. a quantum yield of 8 moles of photons (8 einsteins) captured per mol of oxygen produced (and CO2 assimilated) is assumed. generally falling in the region 0. The reactions following these charge separations give rise to the formation of 3 moles of ATP and Energy Environ. using the above numbers. A quantum yield of 8 (4 quanta at 680 nm and 4 at 700 nm) would have a total energy content of 1384 kJ per 8 einsteins. with a median value in the vicinity of 1 MJ mÀ2 dÀ1. achieved by reducing the size of the light-collecting antenna. The zone between the blue dashed line and the solid blue line for photosynthesis is that of unexpressed enzyme activity. and the energetics are concisely outlined in ref. the energy from the excess captured photons has to be disposed of in some manner. 128). 554–590 | 567 This journal is ª The Royal Society of Chemistry 2010 . A rigorous analysis of the thermodynamics was made in ref. thus the equation simplifies to Pz 0E ¼ E0/k (3) Combining eqn (1) and (3) gives the minimum irradiance for growth Emin ¼ Eckz 0 (4) For cultures with a biomass of 0.

The hatched lines are stages at which the losses are variable. If nitrate is used as a nitrogen source as opposed to reduced sources such as ammonia. 3.2 Â 10À3 2. 2010.6 Â 10À3] 568 | Energy Environ.4] [2. the radiation available for photosynthesis is only some 45% of the incoming radiation. data taken from Table 1). 12. as the losses are determined by the stoichiometry (metabolic losses) and the thermodynamics of the processes – for which there is limited scope for variation. hexoses) to biomass i.64O0. The biochemical composition of the cell will affect both biomass and energy yields. 9).7 12.6 [6. along with the various yield terms are used in the study of the energetics of plant culture. the overall efficiency of the formation of 1 mole of organic carbon from the 8 absorbed moles of photons themselves would be 34%. with a calorific value of 469 kJ molÀ1 C. Values are calculated on PAR except those within brackets. Sci.g. 57. 15 Energy losses during photosynthesis. Thus. This reduces the photosynthetic efficiency to 27% (see Table 5).2 [8] [3. whereas the quantum yield can be remarkably constant across the PAR range. There are also energy losses associated with the metabolic conversion of the primary photosynthetic products (e.1 on ammonia as a N-source and 1.44N0.Fig. 15A and 15B) There are also inevitable energy losses preceding and following these two sets of reactions.13) for a cell containing 42% protein.3 on nitrate.8 Â 10À3 1. incorporating these losses. CHO refers to organic material with a hexose-type elemental ratio. 25% lipid and 5% nucleic acid. 13). A significant change in yield can result from the state of oxidation of the nitrogen source – whether the cells are using ammonia (or urea) or nitrate. The stepwise loss of energy during the production of 1 mole of organic carbon as glucose (calorific value taken to be 469 kJ molÀ1 C). with a calorific value of 541 kJ molÀ1 C (24.e.2 Â 10À3] — — CHON (NO3) 14. This loss will be dependent upon two factors. with the major part of the loss occurring during the light reactions (see Fig. Table 5 Calculation of maximum photosynthetic efficiencies.7 kJ g À1. B. then the reduction of nitrate calls for extra energy.3 5. The above efficiencies may be regarded essentially as fixed ceilings for photosynthetic efficiency under natural conditions. 14). reducing the overall yield to 12%. Photons are gathered from across the whole 400–700 nm range – the balance will depend upon the photosynthetic pigments present in the cell. and a calorific value of 469 kJ molÀ1 C (15. This is discussed in Box 1 and the effect of varying cell lipid content is illustrated in Fig. The fractional energy losses at the major steps during photosynthesis. would reduce the overall maximum yields to 8% after respiration is considered. This gives photosynthetic quotients (DO2/ÀDCO2) of 1. 3908 kJ of incoming radiation is required to produce one mol of organic carbon.1 10. the overall yield of the incoming radiation is reduced to around 10%.7 7.8 8 CHO [12] [7. A quantum requirement of 10. characteristically increasing the energy demand by 20–30%. where there may be possibilities for manipulation of the photosynthetic apparatus and/or cell metabolism: (i) concurrent respiration (Fig. These products of the light reaction in turn give rise to the formation of 1 mole of organic carbon with an elemental composition of CH2O. polysaccharides. This loss is about 20%. Taking this to be a hexose. There are two further forms of loss. lipids. 28% carbohydrate. 554–590 This journal is ª The Royal Society of Chemistry 2010 . 2 moles of NADPH a combined yield of 590 kJ. A summary of photosynthetic yields calculated from the present analysis. proteins.6 kJ gÀ1). energy losses will be incurred transferring the energy to the lower frequencies of the longer wavelength photons (see Fig. CHON refers to the calculated carbon-normalised major element composition (C1H1. which are variable. Second.. and (ii) photon wastage (Fig. which are rounded off values based on total solar radiation Type of yield Bioenergetic yield (J%) Energetic yield (JkJ) Quantum yield (JE) Photons/mol C fixed Units % (kJ kJÀ1) g kJÀ1 g einsteinÀ1 einstein mol CÀ1 26. etc. A.7 Â 10À3] — — CHON (NH3) 17. is given in Table 5. Yield terminology and symbols adopted from ref. rather than 8. Taking a median estimate of the 24 h loss to respiration as 20% of photosynthesis.7 17 Â 10À3 3. First.

com/photos/jurvetson/58591531/). (ii) photobioreactors (PBR). 18A and the more cautious quantum requirement of 10. 18A. the same as in Fig. We return to this problem in the following section. Energy Environ. vertical coils or columnar structures as well as flat plate structures. 4. mid 220. They may take the form of narrow tubes. Eilat. Photon wastage is the principal reason why the actual yields fall short of the theoretical.7 kJ gÀ1 dry weight (see Table 5) and a respiratory loss of 20% Maximum biomass yield/tonnes dry weight haÀ1 aÀ1 Crop Higher plants Theoretical* (C3 plants) c% ¼ 4. although not invariably. algae unspecified Achieved bioreactor (Phaeodactylum) Achieved raceway (Pleurochrysis) over 10 months Source Low 210. high 280*** 110–220 175 127 120–153 182 60 54 54 67–68 19. when attempting to maximise the output from mass cultures of algae. 58). 16) are simple engineering developments of the pond/tank type system. we consider the theoretical limitations to biomass production. Bioreactors (see Fig.7 Low 410. high 140** Low 270. they are oval in shape with depths 100–300 mm and the water is kept in circulation with paddle wheels – the most energy efficient system. algae unspecified Projected raceway. often having internal dimensions as little as 30 mm.1.0% Sugar cane Switchgrass Corn (grain) Poplar wood chips Soya Rape seed Oil palm Microalgae Theoretical c% ¼ 12% (Table 5) Projected raceway. high 190** 74–95 8–20 8–34 11 4. 554–590 | 569 . 2010. 3. mid 170. two types of growth system have evolved: (i) raceways. then. 17 Photobioreactors (Greenfuels image courtesey of http:// www. theoretical values are given for three latitude zones. subsidiary of Nikken Sohonsha Co.5 4. closed bioreactors and open ponds. photon wastage (which can be up to 80%) being the major problem.67 66 69 66 66 66 Present account 16 4 4 9 70 71 Fig. frequently with some form of agitation. algae unspecified Bioreactor raceway. ** assuming a calorific value of 20 kJ gÀ1 dry weight for the crop as a falling to 280 tonnes dry weight haÀ1 aÀ1 (75 g mÀ2 dÀ1) at latitudes 45–55 . Production rates: background and observations Building on the background information on photosynthesis. characteristically. At their simplest.6% Theoretical* (C4 plants) c% ¼ 6. the maximum ‘‘theoretical yields’’ of a carbohydrate type molecule would be 410 tonnes dry weight haÀ1 aÀ1 (112 g mÀ2 dÀ1) at low latitudes less than 30 . allowing for respiration. This journal is ª The Royal Society of Chemistry 2010 Fig. the difference being due to the greater respiration losses in higher plants. If we take the irradiance information used to create Fig.Table 6 Observed and projected yields for crop plants and microalgae. * allowing for respiration. Actual yields (see Table 6) fall short for a number of reasons. with a light capturing depth of less than 100 mm. Gifu. horizontal or inclined tubes. The former (see Fig. algae unspecified Best case raceway.6 to 6%.5–6 8. We discuss two types of algal biomass production systems. This phenomenon continues to tax the ingenuity of researchers and engineers and is far from resolved. mid 330. based on the incoming radiation and efficiency of energy transfer from photons to biomass. 24. Many of the financial disasters in mass culture of algae have been associated with bioreactor-based systems (see ref. 16 Open ponds (image courtesy of Nature Beta Technologies Ltd. Initial work on mass culture of algae was carried out in ponds and tanks of various forms. From these beginnings. Japan). Figures for annual insolation are calculated as for Fig. *** assuming a biomass calorific value of 24.. 17) are enclosed systems of various geometries. Sci. Israel. Algal growth and production By comparison the estimated equivalent yield for higher plants54 (see Table 6) lies in the range 4. The main problems with algal culture in bioreactors are the maintenance of the necessary turbulent flow in long lengths of narrow tubing and the possibility of inhibition of 4.6–5.

a temperature maximum and a temperature optimum. giving broad nutrient-limited and nutrient-unlimited zones. The first is respiration (R). is high at low temperatures and high irradiances. In the case of light. These approaches do not take account of the metabolic work on transformation from hexoses (taken as the primary photosynthetic product) to other biochemicals. 50 000 kJ molÀ1. This journal is ª The Royal Society of Chemistry 2010 . Strictly a correction should be made to the reported bomb calorimitry values for the heat of formation of ammonia from dinitrogen (46 kJ molÀ1) otherwise the DG of the reaction will be overestimated. after which the cultures are periodically flooded into large area raceways. as ash-free dry weight (per unit area or volume).e. It is debated whether growth is controlled by the most severe limiting factor or a product of all factors at one instance in time. 56) this is calculated theoretically from elemental composition or established empirically by bomb calorimetry. where a pure culture is maintained.60 4. Sci. which essentially subtracts from growth (m).photosynthesis due to the accumulation of oxygen in the closed system. 18A. Temperature is different to nutrients and light. A number of equations have been devised to model this latter curve (see ref. bioreactors. 18B are for a ceiling value of bioenergetic yield of 10% this is obtained by correcting the 12% yield for a hexose (Table 5) for a 20% loss due to respiration. The error is small. are given in Fig.2. Given this. The overall temperature response has three cardinal points – a temperature minimum. Yields 4. There are also physiological interactions between the responses to temperature and light. Active pumping with air-lift pumps induces turbulence and also helps to drive off the accumulating oxygen.4 kJ gÀ1 in the case of protein and 0. The curves given in Fig. reduced by one or a combination of growth limiting factors – the two key ones in the case of the algae are light and inorganic nutrients (e. Such systems have been successfully used for growth of the astaxanthin-producing algae Haematococcus pluvialis. Further.2 or less in the case of algal biomass. as without exception. then a simple linear calculation of organic production may be made from the product of the irradiance and the energetic yield (see Table 5). In these coupled systems. of which some 50% (500 J mÀ2 sÀ1or 2300 mE mÀ2 sÀ1) lies within the PAR region. 19.g. Maximising the output of these systems. Characteristically the effect is non-linear.3.: Production (M LÀ2 TÀ1 or M LÀ3 TÀ1) ¼ biomass (M LÀ2 or M LÀ3) Â growth rate (TÀ1) Biomass may be expressed as moles or mass of organic carbon or. as well as the immediate response. The calculation of incoming radiation is as follows: with a clear sky. more commonly in algal mass culture. it is possible to calculate maximum ‘‘theoretical’’ yields of biomass per unit area for various latitudes and times of the year.7. the relationships are non-linear. The calculated daily irradiances for various latitudes are given in Fig. derived from satellite observations. Finally a correction is made for reflective losses from the surface of the water using Fresnel’s equation – although this correction is very small. about 0. 300 mm) bioreactors act as a ‘‘nursery’’ stage. From the information derived in Section 3 (summarised in Table 5) and the calculated incoming radiation.. giving effective 570 | Energy Environ. algae also have some capability to adapt to the ambient temperature. this particular calculation is intended to provide nothing more than a high ceiling value. field data of total incoming radiation. for a number of reasons. 2010. chemical and biological factors. whereas the enzymatic system is temperature sensitive. Biologists customarily use a simple logarithmic alternative to the Arrhenius equation – the Q10 – defined as the change in rate over 10  C – the value is characteristically close to 2. activation energy of ca. To transform the energy yields to mass yields (i. being closed. Two additional factors affect the growth rate of algae. The point made by this latter figure is that local atmospheric conditions – notably cloud cover – give rise to a much more complex distribution in space and time of incident radiation than the simple calculation from which Fig.16 Microbial production (or yield) may be regarded as a product of biomass (crop) and net growth rate i. Details and the overall calculation may be found in ref. This is modelled by the biological equivalent of the Langmuir isotherm (Michaelis–Menten equation). as the photochemical system is essentially temperature insensitive. Once the irradiances have been obtained. which serve as the ‘‘grow-on’’ phase. both are of considerable importance in modelling and designing growth conditions. 554–590 (i) ‘‘Theoretical’’ yields. with the number of interacting factors is complex. On the positive side. the incident solar radiation with the sun vertically overhead may be taken as 1000 W mÀ2. the irradiance may be calculated for each hour angle of the day and for the cycle of the solar declination angle through the year. Relevant to outdoor mass algae culture (and in common with light). For comparison purposes. 14). Photoinhibition. carbon or phosphorus). 47 and 61. Growth rate is subject to a number of modifying physical.e. whereas the starting and end nitrogen compound in microalgal growth is commonly ammonia. One must stress that.e. in that it is treated as a determinant of mmax. The zone from the temperature minimum to approaching the temperature optimum closely follows the Arrhenius equation. nitrogen. A coupling of the above systems has been used and found to be very reliable and successful. large diameter (ca. Controls on algal growth Growth of microorganisms is usually modelled as a speciesspecific maximum growth rate (mmax). kJ to g dry weight) an energy/ mass conversion factor is required. Commonly (see ref. 57 and 59). 18A is derived. with probably only a single exception (the apparent Arrhenius constant in the temperature response curve). and associated losses.xx A more correct value may be derived from the xx Bomb calorimetry involves the conversion the nitrogen in the molecule to dinitrogen. with the initially controlling factor reaching a point where it no longer affects the growth rate.: mnet ¼ m À R The second factor is temperature. there is a further zone of light inhibition (see Fig. rather than a moderator. are much less prone to contamination than open raceways. and is customarily ignored. i. the values for the parameters cannot be anticipated from theory with any degree of certainty. 3.

64). Variation of calculated productivity with latitude. 20A summarises an extensive collation of reports of area yields of algal biomass derived from various culture systems. Monthly averaged ‘‘theoretical’’ daily productivity (as dry weight) through the year at various latitudes again using the same tanh relationship as insert C. Furthermore. Fig.7 kJ gÀ1. D. 2010. Sci. a 3% yield (an average obtained value. eqn (5)). some 19 sets of observations in total and predominantly from high performance Energy Environ.7 kJ gÀ1) through the year at various latitudes. assumed calorific value 24. The calculation assumes that only light limits growth – no consideration is given This journal is ª The Royal Society of Chemistry 2010 . 5. Fig. 554–590 | 571 Fig. 20B (a geometric mean has been used to avoid biases due to the wide scatter). 20) and the above tanh relationship. 18 A. as there have been improvements over the years. and separated into ponds. The former can be estimated from either the protein/ polysaccharide/lipid content (see Box 1. assuming a fixed protein/carbohydrate ratio of 3 : 2 (Box 1.4 (i) and Fig. C. no biological losses. The clusters of low rates (>20 g mÀ2 dÀ1) for raceways in the post 2000 period come from observations during the solar winter at latitudes greater than 30 . 12. In Fig. This is not anticipated from the radiation calculations and may be due to temperature limitation arising from evaporative cooling effect on the raceways (see the following section). as they appear close to or beyond accepted ‘‘theoretical’’ yields. B. bioreactor systems and raceways. composition as in Table 5. see Fig. The reported rates have been plotted against time. 65.. The means of the maximum and average/sustained rates are given in Fig. 18D shows the results of a calculation using a non-linear relationship between photosynthesis and radiation – the tanh relationship between photosynthesis and irradiance (see discussion in Section 4. 3. 19 Global distribution of total incoming radiation through the first half of the year. 47 and 61.62 mass of hexose required to produce a given mass of biochemical and the calorific value of hexose itself (taken as 15. 22. 63. Ignoring the low cluster (see above) there would appear a general upward drift due to improvements with time to a figure in the region of 35–40 g mÀ2dÀ1 – very much the prediction in ref. ref. The calculation takes into account the loss from the surface due to reflection. The 3 : 2 ratio for the protein carbohydrate proportions comes from the analysis of data in Fig. the calculation (see text) is based on a 10% bioenergetic yield (see Table 5). assuming 3 and 10% bioenergetic yields (again no biological losses are taken into account) and also using the tanh relationship shown in Fig. Generally values above 40 g mÀ2 dÀ1 come from narrow path length (<50 mm) bioreactors. Where the appropriate information is available. Estimated monthly averaged ‘‘theoretical’’ daily photosynthesis (as biomass dry weight. Two exceptionally high rates (130 and 174 g mÀ2 dÀ1) have been omitted. to control by other factors such as temperature or inorganic nutrients – so in this respect the rates obtained perhaps are best regarded as maximal ones. 20C). Monthly average daily clear sky total isolation for various latitudes. The data set however is very small. They have been further separated into average (or sustained values) and maximum values. (ii) Observed yields.Fig. the bioenergetic yield (j%) has been calculated (see Fig. respiration or organic excretion are taken into account. which will result in a depression of the yield (see Box 1) and Fig. the calculations are made for a 10% bioenergetic yield. eqn (4)) or from the lipid content. Calculation made following ref. unless major improvements can be made to the light capturing system. 21). 18C the data has been integrated through the year giving the distribution of calculated annual yields with latitude. some of the data come from high lipid algae.

the major challenge to maximising the productivity of mass cultures (see Section 4. as the fraction of the light emerging from the culture is a very small proportion (<10À4) of that entering. n ¼ 4). 554–590 . When better sets of data become available. a is the initial slope. 4. turbulence. photobioreactors. B. Upper line is the standard deviation. 21 and 22 show the sets of data we have been able to locate. n ¼ 15) and total solar radiation (TSR. At first sight there would appear to be a significant difference between the rates in raceways and PBRs (as seen also in Fig. 20B and C) but in ref. the algal crops 50–150 tonnes. further controls may be set by carbon dioxide concentrations. We found it necessary to allow for an offset on the irradiance axis. see ref. But this is not the full story. Table 6 sets out yield data for crop plants along with those available for microalgal cultures. it may be that the longer growing period in the case of higher plants results in respiration taking a higher toll on the yields. PBR: photobioreactors. In round figures. bioreactors and raceways. The tanh model was chosen as it provides a direct parameterisation of the initial slope (a). data for a full year). The former loss can be essentially disregarded with cultures with light paths of 100 mm and biomasses of 1 kg mÀ3. light. grouped according to type of growth system. Colours designate the type of system. Given the above efficiencies. 20 A.3 and Table 5). RW: raceways. the yields commonly achieved in outdoor mass culture systems lie between one tenth and one third of the ‘‘theoretical’’ value of 10% of the energy in the total incoming radiation (cf. In Section 4. The resolution of this problem has been. Sci. with these values being around 30% and 10% respectively of the ‘‘theoretical’’ yield (see Table 5). E the irradiance. the mean for raceway observations is much lower at 2%. It is also likely to be 572 | Energy Environ. However. The basis for the difference. although striking. a large fraction (60– 90%) of the incoming radiation is not used for photosynthesis. which allows the overall relationship between daily irradiance and production rates to be explored. is not wholly clear. the reported crop (e.70. Average (geometric means) production rates of ponds. Reported or calculated bioenergetic yield (j%. In part. from which the photosynthetic efficiency (j%. plus the PAR values corrected to TSR values by dividing by 2 (see Section 3.g. 3. Data and sources given in Appendix IV (provided in the ESI†). see Section 3. The fitting to the data was undertaken using a least squares analysis. 2010. There is a paucity of reported data on the seasonality of production rates for PBRs and raceways. compared with bioreactors.72.1(i)). and the below-ground yield (roots) is almost inevitably omitted.5(i)). crosses maximum rates. The data have been separated into PBRs and raceways. There are major uncertainties with the estimations for algal biomass yields in that there are very few reports of long time series (i. 47. based on photosynthetically available radiation (PAR. temperature and oxygen were identified as factors that would affect photosynthesis.. We simply have to wait and see. Table 5 and Fig.4 Controls on yields Broadly. we may find some downward revision of the numbers. A number of factors give rise to this. and continues to be. C.e. In order to calculate the photosynthetic efficiency. The generally lower values for raceways. The ‘‘theoretical’’ maximum is taken from Table 5 allowing for 20% respiration. inhibitors and contamination.due to the fact that. whereas those in remaining 90–95% of the culture are severely light limited. Fig. Analysis of published production rates of outdoor cultures. in the case of the higher plants. Some 50% of the total incoming radiation is outside the range useful for photosynthesis and so cannot be used. solid circles sustained rates. but more likely that the bioreactors are far less susceptible to contamination and the populations in raceways may be growing sub-optimally.73 The relationship between light and areal production rates was analysed using the tanh model for the PvE relationship (P ¼ Pmax*tanh(a*E/Pmax). where the mean bioenergetic yield (based on PAR) is close to 10%. 72 the This journal is ª The Royal Society of Chemistry 2010 Fig. 20C). this may be offset by improvements in strains and culturing techniques. a calorific value has to be prescribed for the organism. (i) Light. lower the standard error. ‘‘TSR’’ is the TSR efficiencies.1. may in some part be due to design limitations. The main loss is associated with the wastage of photons after absorption by the algae. which results in the culture as a whole using light very inefficiently: the algae in the first 5–20 mm of the light path being light-saturated or light inhibited. grain) may only be part of the above-ground plant yield. where Pmax is the maximum photosynthetic rate. the higher plant annual yields fall generally in the range of 5–30 tonnes crop dry weight per hectare (sugar cane being the striking exception). this was calculated from the reported lipid content for the organism and the calorific values reported in Table 1. Losses may result from light not being collected by the culture or that the photons collected by the algae are in large part wasted and their energy is lost as heat or fluorescence. see Table 5) may be calculated.

but that data set lacks observations at the low irradiances needed to establish whether or not there is an intercept. organism cultured: Phaeodactylum tricornutum. On a daily basis this results in a daily cooling effect equivalent to some 12 MJ mÀ2 (ca.Table 7 Parameters derived from the analysis of data shown in Fig. as there will be some moderating feedback between cooling and evaporation – but as evaporation rates are proportional to degrees Kelvin.3 3. Most important is low spread of values for the initial slope (a). so it cannot be the sole explanation. this would give rise close to a 4-fold reduction in metabolic rate and possibly a shift in the photosynthesis/respiration ratio.9 Æ 1.72 of the seasonal changes in biomass yield in outdoor photobioreactors. thus the observed offset may be a combined effect of temperature and irradiance. The data in Table 7 have been used as the basis of parameterisation for the production model used elsewhere is the review. 554–590 | 573 Fig. The derived parameters from the analyses and the photosynthetic efficiency and its calculation are summarised in Table 7 and a number of features are worth noting.5 16 23. 21. Other details as Fig. The study in ref.5 in ref.0 4. allowing for a 20% loss incurred as respiration. 71.3 9. The derived parameters are given in Table 7. With 150 mm deep raceways this generates a potential cooling of 20  C per day.5 24. where P is the observed rate of photosynthesis. ref. It does not seem practical to use solar panels as heat collectors to offset the heat loss due to cooling. Water temperature also varies with irradiance and will have an effect upon photosynthetic.9 PBR 60 70 86 3. E the irradiance. 70 was undertaken in southern Spain at a latitude 36 480 N. in the data from ref.3 to 9.5 0. same organism was grown in parallel in PBRs and raceways and the rates are essentially identical. the mean value is 2. or perhaps absent. 21 and 22. but an offset on the irradiance axis (Emin) allowed. The second important outcome is the apparent irradiance offsets (3. This offset is not as evident.72 of the seasonal changes in biomass yield in outdoor raceways. the data were fitted to the tanh expression P ¼ Pmax*tanh(a*(E À Emin)/Pmax). (ii) Temperature. 2010. 72 study was made in central Italy at 43 80 N.4 and Table 14. see Fig. and respiration rates. 22 Analysis of two data sets71.8%.5 25. 14. 21 Analysis of three data sets70. Pmax is the maximum photosynthetic rate.3 5. The study in ref. 74 (see Fig. as the incoming radiation (10–25 MJ mÀ2 dÀ1. organism cultured: Pleurochrysis carterae Growth system Dimensions/mm diameter or depth Reference Pmax/g mÀ2 dÀ1 a/g MJÀ1 Offset/MJ mÀ2 dÀ1 Lipid content (% dry weight) Calculated calorific value/kJ gÀ1 Observed photosynthetic efficiency (J%) PBR 30 70 1400 1. 3. A temperatureparameterised model would be needed to resolve this. 71. The incoming radiation has a marked diurnal effect upon the temperature of the systems.1 RW 150 72 20 1. Evaporative losses at middle to low latitudes fall in the region of 2 m per annum.4 Æ 0. This journal is ª The Royal Society of Chemistry 2010 .9 3. 70.2 PBR 35 72 20 2. Clearly supplementary heating is impractical. distinctly below the observed range of 3–9 MJ mÀ2 dÀ1. Sci. a is the initial slope.3 26. 76 observed 10–25  C increases in temperature during the day due to solar heating. The matter is clearly more complex than this.3 8. 74).0 7. In the case of shallow open systems there is a counter effect on temperature due to evaporative cooling. Thresholds. 18A) is. 300 calories cmÀ2). not too dissimilar from that associated with the evaporative associated losses (12 MJ mÀ2 dÀ1).6 26. The irradiance data were obtained from the Australian Bureau of Metrology database. as the energy required would far exceed the energy gain from photosynthesis. a value for the primary photosynthetic efficiency of 7.75 g MJÀ1 gives a calculated photosynthetic efficiency of 5. were reported for mass cultures in ref. ref.7 22. 70.7 À4. The simple explanation for the threshold would be that it represents the compensation irradiance (see Section 3.7 MJ mÀ2 dÀ1) seen in the data of ref. ref. the feedback will be weak. so the apparent differences may be more due to the organism or the environmental or operating circumstances. very close to the theoretical value of 8% for the production of biomass (see Table 5). The study in ref. 75.47 The lines were not forced through zero. 71 was undertaken in Perth in Western Australia (latitude 31 570 S). the culture organism was Phaeodactylum tricornutum. the plot for the 30 mm PBR certainly looks anomalous.2) but an analysis for dense cultures (see Box 2) suggests this would give rise to a maximum value of 2 MJ mÀ2 dÀ1. 72 and 73. Given a Q10 of 2. 72. Using a least squares analysis. equivalent to 5–9 MJ mÀ2 dÀ1. as it should be. Temperature is very likely a major factor determining the productivity of outdoor growth systems open to the atmosphere and may limit the latitudinal extent to which they can be successfully used.. the culture organism was Tetraselmis suecica. organism cultured: Tetraselmis suecica.4% is obtained.5 Fig.5 25.6 RW 150 71 41 2. the organism cultured: was Pleurochrysis carterae. furthermore.2 16 23. so the heat Energy Environ. Sources: ref.9 4.

allows the slower enzymatic reactions to catch up with the photochemical reaction. Ref. Ref. Consider the example of seawater. Photosynthesis occurs as three events with badly matching time responses:84 photon capture rates have timescales of 10À6 s or less. is complex and beyond the scope of the present review.05 m sÀ1 ensure this. the dark period needed to be 10 times greater than the light. Whether such systems can be made economic remains an open question. maximising the photosynthetic efficiency. oxygen may be calculated to accumulate at rate of about 4 mol mÀ3 hÀ1 (ref. giving light attenuation coefficients of $200 mÀ1) and supraoptimal irradiances. At these flow rates. the algae are presented with a very unnatural situation and they are not equipped physiologically to deal with it. 2010. whereas downstream enzymatic carbon assimilation can process at best 100–200 electrons per second. This journal is ª The Royal Society of Chemistry 2010 . Seawater total inorganic carbon dioxide concentrations are approximately 2 moles mÀ3. to have a significant effect. (iv) Carbon dioxide. thus reaching inhibitory concentrations in 20–30 min. Ref. At daily production rates of 30 moles mÀ3 (see above). where h is the depth and u is the velocity. Part of this derives from the competing oxygenase activity of RuBisCO (see section 3. Ref. see the following section). and are equivalent to bioenergetic efficiencies (based on total incoming radiation) of 5. as implied before. Thus with open raceway systems.05 Â u) z 30Âh2/u. as the driving force of the reaction is associated with the dissolved CO2. these rates are the highest achieved with raceway cultures. between the flashes.15. 80 undertook a very detailed study with dense algal cultures (3–6 kg mÀ3) and found the flashing light effect to cut out at about 10 Hz. with a high value of 9. Mixing by inducing turbulence alleviates the problem to some extent but would not appear to solve it fully. turbulence cycles the cells through a dark/light cycle. accompanied with a rise in oxygen concentrations from 0. We restrict our focus on maximising the utilization of photons.9 mM. accumulation of oxygen should not occur. all in SI units. This has long been seen as crucial to the success of algal biomass production. which should strip off the accumulating oxygen. A full discussion of maximising the overall output and economy of algae biomass/biofuel production. maximum rates in the region of 60–70 g mÀ2 dÀ1. ref. The rate of CO2 replacement is about one tenth that of oxygen. 77 for growing cultures and 574 | Energy Environ. In essence. 4. where perhaps 90% of the culture is in effective darkness. Ref. provided the system is turbulent (flow rates in excess of 0. The gains in efficiency are lost at flash periods shorter than 10 ms. the root of the problem is that. Oxygen is a by-product of photosynthesis and it has been long known that high oxygen concentrations inhibit photosynthesis (the so called ‘‘Warburg’’ effect). The consequence is that re-carbonation of the water by simple exchange with the atmosphere will not sustain the rates of removal.5%. 60 gives a figure of 6 mol mÀ3 hÀ1 for Spirulina). Oxygen concentrations in the region of 400% saturation (ca. using the same arrangement. the carbon dioxide species in seawater will be exhausted within an hour of so. i. which is only a minor component of the seawater carbonate system.5 to 1 Hz.. The optimum dark period is temperature-dependent but generally falls in the region of 50 ms.06 Â 0.06Âu*xh) ¼ h2/(0. which gave rise to a two-fold or more gain in areal production.78 The problem is peculiar to mass algal culture.1 Hz. With the exception of a couple of questionably values. thus the CO2 needs to be replaced continuously by the addition of gaseous or liquid CO2. 81 concluded that the response in outdoor tubular bioreactors saturated at frequencies greater than 1 Hz.e. however. (iii) Oxygen. 79 extended the early studies in ref. The exchange of gases across the air/water interface results in some 20 cm depth of water being re-aerated per hour. Near ‘‘theoretical’’ yields can be achieved in short light path lengths of dilute cultures at low irradiances. 60 reported that a fall in temperature from 35 to 25  C. The consequence is that 90% of the photons are absorbed in the first 10 mm by algae suffering severe light inhibition and so use photons very inefficiently – wasting perhaps some 80–90%.5 Maximising yields (i) Maximising biomass yields. Sci. Mass algal production involves optically dense cultures (biomasses $1 kg mÀ3.15–0.collectors would need to be broadly of the same area as the growth systems and would almost certainly not be economic.78 The dark period. 2 mM) essentially switch off photosynthesis. There has been extensive theoretical and experimental work on this effect. In the case of enclosed bioreactors. but exists in virtual darkness.5%. 554–590 showed that.06Âkz) ¼ h3/(0.69 mM to 1. in raceways 150 to 200 mm deep. The supply of CO2 could well be a major constraint on the siting and consequential scale of algal biomass production facilities. There is apparently a combined effect of temperature and oxygen. 3. well in excess of the 2 mM inhibitory level. these rapid rates of oxygen production impose constraints on the maximum length of run and the minimum flow rates within the bioreactors. 83 report sustained production rates of 40 g mÀ2 dÀ1. the cross transfer frequency due to turbulent diffusion would be of the order of 0. Thus the remaining 90% or more of the culture is using photons very efficiently. In a subsequent paper. Bioreactor systems characteristically use airlift pumps to circulate the water. 74 concluded that power consumption considerations would limit flows to 0. In dense cultures.1(ii)). Many of the details for oxygen are shared with carbon dioxide. 82 used simple hydrofoil spoilers to induce turbulence and with a raceway system was able to achieve a mixing frequency of 0. It had been demonstrated early on in the study of the mechanism of photosynthesis that the yield of oxygen per photon was greater in intermittent light. with short term. gave rise to a substantial (60%) fall in photosynthetic rates.2 msÀ1. where there is a broad chemical predictability.77 The basis for this is that a single 400 chlorophyll photon collector can process some 2000 excitations per second. although the implications are profoundly different. in mass cultures. Commonly encountered photosynthetic rates in mass cultures (ca. (v) Turbulence. 700 g dry weight mÀ3 dÀ1) result in net oxygen production rates of 30 mol mÀ3 dÀ1 or a rise in oxygen concentrations of 30 mM over the daylight period. Ref. consistent with the above generalisation on relative processing rates of the photochemical and enzymatic reactions.{{ thus there is potential for improvement of production rates by increasing the turbulence in raceways. whereas enzymatic CO2 fixation and reduction have {{ This is calculated as the transverse timescale ¼ h3/(0.

15. but this is not achieved in the case of photosynthetic system I. algae adapt by reducing the size of the light harvesting antennae and so reduce the rate of collection of photons. has long been seen as the more likely solution (e. The results from a simple spreadsheet model show that if the chlorophyll content is reduced.88 importantly without apparently compromising enzymatic capacity and there appears to be no penalty due to rise in respiration rate. it extends culturing time and increases the space and capital requirements of the production plant. 86). 6 implies that an increase in lipid content from 15 to 30% would give rise to a 50% or greater reduction in growth rate. we estimate there to be around a 2. An alternative approach to producing lipid-rich cells is to drive the cells into nutrient deficiency. resulting in a more efficient photon usage and greater areal productivity. the probability is that another enzyme would then become limiting and the problem would end up processing through the complex cascade of enzymes of the dark reaction. the analysis made in ref. by reducing the photon capturing capacity. When exposed to sustained high irradiances. Thus. Unfortunately this work was in its infancy when the ASP was terminated. In combination.g. unless the high irradiances are sustained. The cautious conclusion is that given these developments one could reasonably expect to approach 50% of the ‘‘theoretical’’ efficiency.3. (ii) Maximising lipid yields. First. a greater number of photons are delivered to the deeper parts of the culture. when lipid accumulates (see Section 2. so a priori the two approaches to improving the utilization of This journal is ª The Royal Society of Chemistry 2010 photons cannot be expected to be complementary.g. Even if one were able to engineer improvements in the reaction rate of RuBisCO. ref. Increasing their lipid content. it is unlikely that one will be able wholly eliminate the problem. If the economic analysis focuses exclusively on biodiesel and lipid production. nucleic acid or carbohydrate) must decrease. This was a major research thrust of the US Aquatic Species three-fold. The effect is most pronounced at intermediate irradiances and as a consequence higher latitudes. 3. the algae exist in a rapidly fluctuating light regime making it impossible for them to adapt to the high irradiances. so the feasibility of raising lipid yields by such means has not been fully explored. as the fraction of lipid is increased some other cell component (e. It is possible to mix the culture on time scales of fractions of a second. it does not solve the fundamental problem. no associated increase in lipid levels was found (see ref. the first was to isolate and screen algae for high lipid producers. Broadly. 3. however. At the present it would appear that there is limited potential to increase the lipid content of the algae and for a number of reasons 35% lipid content appears to be a realistic maximum target. However. but not on the required microsecond time scale. This simple model suggests that 2-fold gains in photosynthesis can be expected. At first sight a logical strategy to improve the economy of algal biodiesel production would seem to be to obtain and grow algae of high lipid content. so although mixing will alleviate the congestion in the electron chain to some extent with a consequential increase yield. or modify the cell to produce more. The coefficient of relationships shown in Fig.6-fold reduction in biomass during the synthesis of microalgal cell lipid from a hexose – this effect can be seen in the yield calculations for cells of varying lipid contents in Fig. This is analysed in Box 1. The reduced growth rate is accompanied with a proportionate increase in the period the organisms would need to be held in the growth system and a consequential increase in costs. The proteins and nucleic acids are major determinants of maximum growth rates. An apparently unrecognised penalty of growing algae of high lipid content is the significant overall biomass loss that necessarily occurs when lipids are synthesised from the primary products (hexoses) of photosynthesis. The problem is that the time-scale of the adaptation is long as compared with the other timescales in photosynthesis and relies upon the algae being held for periods of tens of minutes to an hour or so at high irradiances. however. It had been possible to increase the level of expression of the enzyme two. In mass culture. 78). However. 554–590 | 575 . ref. by driving the algae into nutrient deficiency. and it is far from clear how these biochemical groups change as lipid content changes (see Fig. The enzyme acetyl-CoA carboxylase. 49 would appear to show this assumption to be false. 138). There are. Furthermore. the algae appear to revert back to the low light/high chlorophyll state. It has been possible to down regulate these proteins and so reduce the photon capturing ability of the algal photosynthetic system (see e.86. apparently inefficient enzyme RuBisCO has been an obvious target based on the supposition being that one could improve on evolution. penalties in producing cultures with high lipid content. Solving the other end of the problem. 23. However. Fig. Improving productivity of the culture in this way probably negates some of the gains that can be achieved by mixing. 5). a further third is lost as CO2. There is a 50% loss in mass resulting from removal of oxygen during triglyceride synthesis.timescales $1 s and the adaptation to changes to elevated light levels even longer timescales $103 s. The solution lies in either speeding up the enzymatic reactions or slowing down the photochemical ones. It is not possible without a sophisticated model to determine the combined effect of these two approaches. The slow working. The photosynthetic unit associated with photosynthetic system II can be reduced some 3-fold from some 300 chlorophyll molecules down to 95.g. is the first committed step in lipid synthesis and was regarded as the limiting reaction. two lines of research were followed. 15. This problem has attracted research interest and headway has been made. p. giving a maximum potential bioenergetic yield in the region of 5%. the adaptive response is far too slow to resolve the problem of super-optimal irradiances. ultimately gives rise to the same problem. protein. Sci. which catalyses the carboxylation of acetyl-CoA to malonyl-CoA. if the components of the cell that are diminished at the expense of lipid Energy Environ. 7).88 The reduction in the size of the light collecting antenna gives rise to 2-fold or more enhancement in photosynthesis and growth at high irradiances. 2010. consistent with the supposition in ref. then this may not be a problem. The second approach aimed to increase the extent of lipid production by identifying the rate limiting enzyme and modify the cell’s genetics to increase its expression and so increase yield.85 The solution is to manipulate the physiological control mechanism and to switch the organism permanently into the high-light adapted state.. and allowing for the different component lipids and their proportions in algae.85–91 The chlorophyll antennae are assembled on a scaffold of so called ‘‘light-harvesting’’ proteins and it is these proteins that set the size of the chlorophyll antennae.

summarised in Table 7. increase are an important part of the economic equation.55 (dimensionless). the dataset from70 lacked the observations at the low irradiances necessary to adequately constrain the intercept. the mean value found in Fig. In order to do this we need to back calculate the rates of hexose formation from the biomass-derived rates. In the model. 72. the effect will very likely be much greater in reality as one may expect additional strong temperature effects on growth. We chose the Moheimani data set as it comes from raceways. 72 are low when compared with the data shown in Fig. The data sets of ref. 64). the trend with latitude derives mainly from the reduction in annually integrated insolation. 12. which derives from eqn (5). Fig. 71 observed a mean lipid content of 36. described in Fig.55 g MJÀ1.7 kJ gÀ1 (ref. 3. This assumes a protein to carbohydrate ratio of 3 : 2. This affirms the need for temperature-parameterised models of photosynthesis and respiration. which was part of the ASP programme.86 MJ mÀ2 dÀ1. and their variation with latitude from the insolation data derived in Fig. resulting in the algae failing to achieve the rates that the irradiance would allow. with no evident seasonal reduction of productivity. This is done by reversing the calculation of the mass loss during the biomass.5(i)). Earthrise Farms in southern California (latitude 33 080 N) only operates its raceways for 9 months of the year. then this loss on conversion could well be a problem. 23 Estimates of algal areal biomass yields (both daily and annual) for a range of latitudes. The initial calculation we make is the rate production of hexose. Box 1. 19). Emin ¼ 5. especially if they were to command a price comparable to or greater than biolipid (see Section 6). 23. Pmax was taken from ref.Fig.9 g mÀ2 dÀ1. this is seen when the economics are considered (see Fig. The initial calculation is of primary photosynthetic production of a hexose. 72 show a mean offset on the irradiance axis of 5. 71 to produce biomass production rates.. This appears to be the case with commercial production facilities. The calculated photosynthetic hexose production rates are then converted to production for biomasses of varying lipid contents (15. 18A) coupled to a tanh model of the relationship between photosynthesis and irradiance. 71. the calculation makes no attempt to anticipate improvements of the light capturing apparatus of the algae which we may expect to occur (see Section 4. and this questions the search for high lipid species for. (iii) Predicting maximum yields. 21 and 22. unless they possess uniquely high intrinsic photosynthetic rates. This (from eqn (5). There is little to be gained at this stage by making a detailed calculation based on observed insolation rates. It can be seen in Fig. The field observation of yields (vertical bars) placed at latitude 20 come from ref.86 MJ mÀ2 dÀ1. The calculations are based on calculated clear sky total insolation (see Fig. which will overestimate the incoming radiation (cf. the irradiance offset (Emin) was derived from ref. there would appear to be diminishing returns with increased lipid content (see also Fig. which was taken as 15.5% of dry weight. The final values used were a ¼ 3. The value for the initial slope (a) was the average of the full data set. Given the above parameterisations. 554–590 observed integrated rates and the predicted ones for algae with realistic biochemical compositions. Shown for comparison purposes are results from three reports of seasonal productivity abstracted from published sources. Thus.88 for the biomass to conversion hexose and scales up the Pmax value from 42 g mÀ2 dÀ1 (Table 7) to 77 g mÀ2 dÀ1 and the initial slope (a) from 2. 16. 71. Ref. the values at placed at latitude 35 come from ref. Fig. The yields for various lipid concentrations are derived from primary hexose production and the lipid content using the eqn (5). 72. Fig. and successful.3(i) and Fig. shows the effect of the cell lipid content on the total biomass and lipid yields from the primary hexose photosynthetic products. 21. ran into problems of snow and ice during the winter period. In essence we have used the calculated clear sky irradiance values (Section 4. whereas the systems at Kanahoe Point on the Big Island of Hawaii (latitude 19 470 N) are operated successfully on a yearround basis. We have attempted to incorporate the findings of this section into a model of algal biomass production (see Fig. the calculation also requires the calorific value for the primary photosynthetic product. 2010. assuming a protein : carbohydrate ratio of 3 : 2. The calculation is made from clear sky radiation data. 71 – the maximum rates in ref. 18A and the results are shown in Fig. 24).92 The experimental facility at Roswell (33 N). we can calculate the yields per unit area. polysaccharides and lipid (see Box 1). 70. which has incurred a loss of mass on converting hexose to proteins. 20A and accordingly were not thought to be appropriate. 35 and 50% of cell dry weight) using eqn (5) in Box 1. Box 1. Box 1) gives a figure of 1. There may be an additional effect due to the reduction in growth rate at high lipid content.16.43 to 3. 18A) and parameters derived in major part from an analysis of the data reported in ref. which it is consistent with our economic analysis (see Section 6). this mean has been used for the calculation. they will give low biomass yields. This journal is ª The Royal Society of Chemistry 2010 . Pmax ¼ 76. 18A and 19) so overestimate growth rates. The parameters used were derived from the analysis of the data in Fig. Sci. 5. This may limit year-round outdoor culture systems to latitudes less than 35 (see also Fig. The longstanding. 23 shows the very marked negative effect of the lipid content on the yields. 12). 63. 23 that there is broad agreement between the 576 | Energy Environ. There is some steepening of the poleward gradient between the latitudes 35–55 . 23). As a counter to this. so the individual values for a and Pmax have to be scaled up to take account of the fact that the observations were of biomass.

we want to highlight the challenges associated with the harvest and processing of microalgal biomass. with an emphasis on the use of flocculation and centrifugation.93–95 5. Fd and gravity. This would be particularly the case if the spent medium were to be recycled. such as cell volume and cell wall properties. it is probable that an extra concentration step (possibly centrifugation) may be necessary because of the relatively low final product concentration. Another disadvantage is the low solids content (i. however the solids need to be removed from the bowl This journal is ª The Royal Society of Chemistry 2010 manually. similarly containing internally stacked discs. This reduces or avoids the need of energy intensive separation mechanisms like centrifugation. An alternative design is the solid bowl centrifuge in which the bowl contains a disc stack. Until now.96. which requires further concentration Energy Environ.2 through 5. Sci. (ii) disrupting the cells. 554–590 | 577 . disadvantages include the species and growth stage-dependent nature of flocculation efficiency. such as cell number. flow rate. A third type of centrifuge is the nozzle-type centrifuge. the potential toxicity of the wastewater fraction and the undesirable presence of metals in the biomass to be processed are concerns that arise and may inhibit their widespread applicability in the microalgal biomass production process. Out of all steps considered in an algal biomass production process.101. or culture characteristics. is also widely method used for harvesting microalgal cells. It has been suggested that this process could be adapted to be the lowest cost harvesting process.15. despite being identified as a high priority for the future R&D. harvesting and processing of the biomass contains the largest uncertainty surrounding cost and effectiveness. biomass settling rate and settling distance will determine the efficiency of centrifugation. personal communication). For algal biomass. synthetic cationic polymers. With regards to biomass processing. However this set-up also requires manual intervention in removing the biomass from the bowl. The separation step in producing algal biomass as feedstock for biodiesel is difficult and inherently more expensive by comparison with oilseed crops. it is also expensive and energy intensive. Centrifugation is the most common method for harvesting algae from large volume cultures and is widely applicable to a variety of algal species. and in which the shape of the bowl is modified so that the conical section of the bowl has evenly spaced orifices (nozzles). The main advantage of flocculation as a harvesting method is the relatively cheap nature of the process and high volume processing.102 Several different types of flocculants can be used: polyvalent metal salts.e. there are three main phases in the preparation process prior to biodiesel production: (i) harvesting of the algae. we briefly discuss the principles behind the methods relevant to the economical process we discuss in section 6.15 However. causing the biomass to collect at the outer part of the bowl.5. An alternative to settling is flotation of biomass.15.. 3. These processes have been largely avoided in past reviews. Flocculation.e. ref. no clear correlation has been demonstrated between flocculation efficiency. Flocculation refers to the aggregation of particles in suspension to form clumps that can overcome the Stokes’ drag force and increase the settling rate. The methods that are most used for harvesting of algal biomass are discussed in this section. and (ii) bridging. This last type is a true continuous centrifugation system with minimal manual intervention98 and could be considered the most appropriate type to harvest the large algae cultures. The relationship at low Reynolds’ numbers for a sphere is described by Stokes’ law: vs ¼ Fg/Fd ¼ 2/9grc2 (rcell À rfluid)/h The settling rate of cells in suspension follows a square relationship with the radius of the cells and a linear relationship with the difference in density (r) between the cell and the fluid and the kinematic viscosity of the fluid (h).1 Biomass harvest Cell harvest we take as the initial 50–200-fold concentration step of the algal cultures yielding a biomass product that can be used for further processing.97 This process is potentially scalable to large-scale algal ponds. However.4). These three types of centrifuges vary in the volume processed per hour. Harvesting and processing of microalgal biomass Before considering the economics of the process (Section 6). A solids content of 20% can be achieved. However.99. This process can operate more efficiently and rapidly than sedimentation or settling and can also achieve a higher solids fraction. depends highly on the biomass type and requirements of the downstream processing (Sections 5. where dispersed air bubbles in the culture adhere to flocs formed during flocculation and cause the cell aggregates to float. 2010.15 However. and (ii) extraction of the lipids from the biomass. culture age and growth phase. causing each chamber to collect particles of a specific size due to the distinct centrifugal forces exerted in each chamber. The operational variables. i. dose and algal taxonomic group.100 Two mechanisms that give rise to flocculation are: (i) charge neutralisation. A multi-chamber centrifuge consists of a number of tubular bowls arranged coaxially. There are three different types of in-line industrial centrifuges: multi-chamber.97 Although this process is effective. All three types are continuous in that there is a continuous flow of culture through the centrifuges. Settling rate (vs) of microalgae is a functon of two forces (drag. the attraction between the negatively charged algal cell surface and the positively charged flocculentl. Fg) and the diameter (rc) and shape of the cells. likely to be a combination of individual methods. when larger flocculent molecules span a distance large enough to adsorb to multiple particles and hence ‘bridge’ the particles. The efficiency and methodology used in these three steps can have a major impact on the economics of commercial algal biofuel production. The low cost of metal salt flocculants make these the more popular flocculants. flocculation rate and efficiency are highly dependent on cellular characteristics. high pH and bioflocculants. nozzle and solid bowl. 15 and centrifuge industry representatives. in combination with centrifugation or dissolved air flotation. with a maximum of 50 to 100 m3 hÀ1 (Table 8. The choice of harvesting methodology. < 10%) of the biomass harvested by flocculation. The biomass is collected in a conical space on the side of the bowl where it is automatically discharged. such as centrifugal force.

pH 9.2 Biomass pre-treatment and extraction of the lipid fraction The harvested biomass (consisting of about 5–20% solids. The cited literature lacked detailed information on. expressed on a 1 m3 hÀ1 basis. Another method for harvesting the biomass is filtration.82 0. b Capital costs presented. f The cost of harvesting using flotation was reconsidered in ref. It has been mentioned before97 that there is not a universally valid (one-size-fits-all) optimum separation process. 5. most of the literature on the economic considerations of harvesting processes has focused on the need for highly purified products for the food and feed industry and waste water purification. 3. e. An exact economic calculation and comparison of methods for harvesting is complex and practically impossible without information on the species chosen.05–1 0. extraction and process details are not discussed. changes in pH in a stagnant culture will induce settling of algal biomass. 37 and 103 respectively.1 [0. maintenance and capital costs and are based on figures from ref.6–0.97 This species-dependent nature of the filtration process makes this less attractive compared to centrifugation and flocculation and will not be considered further. lipid fraction) for biofuels production.51.5–5 20 0. production system and growth stage for harvesting.e.56] — 1. the harvesting process is a major consideration in the set-up of the production process.. for the sake of comparison the calculation uses a 1 kg mÀ3 cell concentration upon harvesting.1 [0.g. 10% ¼ 10 g dry biomass from 100 g of centrifuged paste). where according to equipment and information available in 1996 the cost of harvesting 1 m3 hÀ1 by flotation was 20% of the cost of centrifugation.4 and 0. Assuming a relative cost of 0. where the economic analysis of the complete algal production process is considered. not absolute comparisons. flocculation is often combined in a process with centrifugation to increase the solids content of the harvested biomass. 15. We have summarised the costs published in the literature to date in Table 8. e The cost calculations have been adjusted for inflation and converted into today’s US dollars (conversion factor 1 AUS $ ¼ 0. are at best approximate since these were obtained from earlier reports and simply adjusted for inflation. Because of This journal is ª The Royal Society of Chemistry 2010 Moheimani (2004)103 d. 97.6 or pH 9. Table 8 Summary of comparisons between relative harvesting throughput. However.e Molina Grima (2004)94 Benemann (1996)15 Mohn (1988)97 Molina Grima (2004)94 Benemann (1996)15 Mohn (1988)97 Final product concentration (% solids)a Continuous process? Becker (1994)37 Cost per kg/$ c Relative costs/mÀ3 Capital cost/1000 $ mÀ3 b Settling/autoflocculation Flocculation Flotation (dissolved air flotation) Centrifugation 3-chamber centrifuge nozzle centrifuge solid bowl or decanter N N Y Y N Y N 1–3 7 8 12–27 20 <15 >20 — — 33 — 15 12 4 — — 19–105 — 55 — — — 9 — — — — 11 — 0. The capital costs presented are adjusted for inflation and converted into US dollars (USD. The relative harvesting costs include reference to operating.81 USD).36] 3. certain types of filtration are ineffective for species in the few micrometre size range. which will make the process cheaper.41] — 4. 554–590 a . species and developmental information is largely lacking in the cited reports.91f — 1 0. nozzle and solid bowl centrifugation. Centrifugation is subdivided into multi-chamber.31 for flocculation.Final product concentration refers to the algal biomass dry weight in the harvested product (e. This table contains the bestcharacterised processes and we have compared these on the basis of processing volume. This is largely due to the uncertainty surrounding the effectiveness. The biomass concentration and form will affect (and most likely be dictated by) the downstream treatment processes. 15 and 94.31 0. not taking improved engineering into account. g Current centrifugation engineering allows processing of up to 100 m3 of culture per hour. Furthermore. because filtration efficiency is highly dependent on the size range of the species to be harvested. $) Volume processed/m3 hÀ1 na na 159–1900 15–20g 2. In summary.8 [0. c Values given in brackets indicate the harvesting costs.2 [0. d Values presented are averaged costs of biomass from cultures grown at unregulated pH. In most economic analyses the exact harvest.39 [0.6 [0.08] 5. Dunaliella and Chlorella due to the rapid clogging of the filters. Seeds require very little pretreatment or processing and the oils (mainly triglycerides) are traditionally extracted either by pressing the oil out of the biomass or using an apolar solvent to selectively extract the triglycerides from the biomass. capital and operating costs. extraction yield and the costs associated with the catalytic upgrading of the lipid fraction.68] — — — 1.6 — 1 — — — — — — — — 1 — 0. flotation refers to the separation process based on the adhesion of air bubbles to flocs of suspended algae after which these float to the surface and separation can occur.32] 578 | Energy Environ. The purpose of the overview table is to provide relative costs estimates. Most of the economic analyses published extrapolate the oil extraction procedures from a seed oil extraction process to algal biomass.61 [0.26 0. na – not applicable.24] 1.4–0. As a result. capital and operating costs.g. species application. The harvesting costs are taken into consideration further in Section 6. such as Scenedesmus. However.71 [0. These figures did not include the cost of flocculant.079 g dw LÀ1 cell concentration for ref.5–3 using other methods. and together with large uncertainties on capital an operating costs it makes exact cost comparisons difficult (if not impossible). 2010. applications.8 0. Settling refers to autoflocculation. depending on the harvesting method used) has to be processed further to produce the feedstocks (i. Sci. we could derive a relative harvesting figure of 0.29] 4. assuming a 0. the type and energy requirements of the centrifuges used. The vacuum drum filters and chamber filter press units are most commonly employed for harvesting fairly large microalgae. The application to harvesting biomass for biofuels will not require the stringent product purity that is the case for the nutraceutrical industry.

5.5 Summary From the foregoing discussion it can be seen that there are a number of routes available for the separation and processing of the algal culture. specific procedures will have to be developed. could only occur if the protein and nucleic acid constituents of algal biomass were put to digestion. Despite its obvious benefits. If nitrate and sulfate are absent. Our own analysis of recycling the protein and carbohydrate fractions via anaerobic digestion likewise suggests that after allowing for the offsetting of the cost of electricity from the energy derived from the methane. The remainder of the nitrogen is principally associated with nucleic acids. which may vary between species and with their physiological and growth status. A range of cell rupture techniques. power generation (from anaerobic digestion) is not a major profit centre’’. cyanobacteria are characteristically low in lipid content. Thus. The yield of methane can be high and the energy recovery likewise high. valuable than the biodiesel itself. sulfate and carbon dioxide in that order of preference. carbon dioxide is the main proton acceptor and the products are methane and CO2. filtration).107 However drying is not considered an economical option for biomass pretreatment for a biofuels production process because of the high-energy requirements of the drying process. This is. In essence. a figure of 70% may be calculated from the data in ref. The process that is utilized in the cost model discussed in section 6 includes anaerobic digestion as an option for residual biomass utilization. if not This journal is ª The Royal Society of Chemistry 2010 .3. This class of compounds have limited nutritional value and could usefully be put to anaerobic digestion.10 However. Furthermore. such as temperature. bacteria turn to a variety of alternative proton acceptors to dispose of the protons the organisms abstract from their organic substrates. it is anticipated that this process will be species. ref. The recycling of nitrogen.108–112 However. because the effectiveness of the cell rupture methodology depends heavily on the physical properties of the algal cell wall and thus will change or have to be adapted with particular species used in the culture. growth.114 however.104. no general strategy can be specified.and environmental conditions-dependent. most likely. Anaerobic digestion is a long established technology in wastewater management for the disposal of organic waste and the recouping of energy. If the protein were sold for animal feed. 15.. 24). Ref.94. no such method has been adopted for algae on a large-scale. If available. or at low concentration. Until target organisms have been identified this may have to remain to be the Energy Environ. species like Spirulina (a cyanobacterium) lack a rigid cell wall and are thus easier to disrupt. and without doubt they are major sources of uncertainty in any economic analysis. No systematic study has been undertaken to optimise. 141) ‘‘Thus. For example. Presently. this does not appear to be the case – in the economic analysis undertaken in the present study (Section 6). then there would be very limited recycling of nitrogen.113 Alternatively. the estimates for the cost of harvesting and separating should be seen as best guesses. the economics of anaerobic digestion are not promising. 15 gives a lower figure for operating costs but attribute a higher contribution ($12%) to capital costs. The composition and strength of the cell wall varies considerably across species and throughout the algal growth cycle. were it economic – it would also result in recycling a major part of the cell’s phosphorus (see Table 2). of course. which could aid in the lipid extraction process by avoiding or reducing the use of solvents. If decomposition can be driven to near completion then the process has the potential to recycle the inorganic nitrogen (as ammonia) and phosphate. However. 3.105 One advantage of processing dried biomass is better percolation of the solvents in the biomass.g. of algal biomass has been shown to aid lipid extraction. Green diesel refers to the production of alkanes through for example catalytic decarboxylation of fatty acids. Chlorella sp. such as drying or cell disruption. 2010. 554–590 | 579 Critical to the economic success of algal biofuel production is the use to which the cell co-products are put. applied and costed for an algal production process. A detailed discussion of the methodology and efficiency of these processes falls outside of the scope of this review and can be found elsewhere. 5. there are too many unknowns in the algal biodiesel process to be able to provide an estimate for the cost of this process.4. both have robust cell walls with high cellulose content. and Scenedesmus sp. Conventional biodiesel production occurs via the transesterification of pre-extracted lipids in the presence of an alcohol and a catalyst.106.large differences between algal and seed biomass properties and oil composition. time of incubation and catalyst concentration. as these can be as. Production of biofuels The lipids obtained by the above processes can then be catalytically converted to biodiesel (methyl esters of the fatty acid portion of lipids) or green diesel (deoxygenated fuel derived from fatty acids). Processing of the residual biomass and co-products more. leading to an increase in lipid extraction. rendering the cells difficult to digest or rupture. develop and price the cost of a biodiesel production process specifically for algal lipids or biomass. A detailed costing scheme was developed for biodiesel production from soybean oil.115 It is worth mentioning that the factors determining the yield and conversion efficiency. chemical and enzymatic. although some may be eliminated based on the current state of technology (e. are highly dependent on the nature and composition of the feedstocks. 5. 15 (p. which can be a strong acid or base to produce fatty acid methyl esters.104. mechanical.104. as 80–90% or so of the nitrogen resides with these molecules (see Table 2). In many cases their effectiveness is dependent upon specific features of the algae. Sci. has been described in the literature as applied to oilseeds and algae. bacteria will use nitrate. there is no net revenue from anaerobic digestion (see Fig. thus saving costs and the carbon footprint associated with the Haber–Bosch production of ammonia. in the absence of oxygen. Pretreatment. Alternative pretreatment methods include cell rupture of the harvested biomass. Uncertainties surrounding the optimum strategy for harvest and biomass processing would not be a major concern if the separation stage made an insignificant contribution to the overall budget. harvest and extraction accounted for 15% or so of the operating budget (50% of the labour costs has been attributed to these processes).

8) are almost identical to our estimate ($209 000 haÀ1). if the lipid extraction process is solvent-based. (deriving in part from the low cost of hydropower in British Columbia) whilst their labour costs are around four times greater (indicating that ours may need revisiting). Assigning cash values to these various products (algal lipid. it is difficult to extract the operational costs with any certainty. all costings were made de novo. The potential of the different scenarios on the use of the residual biomass will be discussed in the following section.e. from fresh estimates. The Food and Agriculture Organization (FAO) statistics132 for the prices of animal feed show a broad correlation with protein content. was $20 425 per year. This.e. Economics of biomass and biofuel production Widely varying estimates for the cost of algal biodiesel may be found in the recent literature (see Table 10). the possible effects of materials used during harvesting and processing and it will be some time before a product value will be established. 554–590 discussion of the analysis of scenarios. The aim of this section is not to produce a definitive costing – presently there are too many uncertainties to allow this – but give a basis to examine the pattern of the economics for various management scenarios. All the items we have been able to cost are built into the spreadsheet. A hybrid system. however.1 Parameterising the economic model We have based our analysis upon a recent set of costings prepared for the US Department of Energy’s Office of Energy Efficiency and Renewable Energy118 for a combined photobioreactor (PBR)/raceway system. they will need to be extended to look at. 5). 6. We have approached the problem by setting a starting figure from the expected chemical property of the product.120 However. 116) to produce costings. From this a spreadsheet model has been generated. Our solution to this problem is. so it cannot be taken as a wholly independent analysis – this is also the case for a number of other reports and to some small extent the present one. prior to considering animal feed as an option. comprising a front end PBR ‘‘nursery stage’’ and ‘‘grow-on’’ stage in raceways is used as the physical arrangement as it appears to be the most cost effective option. there are a number of processes we have been unable to cost with any certainty: the processing of the cell debris to separate the carbohydrate and protein fractions and the subsequent isolation and processing of the protein fraction to animal feed. Their estimate for operating The protein is sold as high grade protein-rich material. Furthermore. This has been updated with published costings and from discussions with colleagues in the field. advances in engineering and improvements in centrifuge technology could also alter the costing. An outline of the costings in the model is given in Table 9. however. Recently a comprehensive and thorough review of the economics of algal biomass production report has been prepared for the British Columbian Innovation Council. 103 are recycled from ref. 103 costed a raceway system. toxicology tests will have to be carried out. the similarity in these values is almost certainly fortuitous. amongst other things. Estimating the cost of the necessary CO2 supply is problematic as it will be very much dependent upon the nature of the overall facility. To this end a set of objective costings is needed. There are additional uncertainties surrounding the harvesting step. 16. Their analysis was not available when our spreadsheet was generated. 6. However. rather than to put in a costing that is circumstance-specific. Without doubt it can be added to and improved upon. protein and carbohydrate plus protein mix) has to be a matter of speculation as no market exits for them as yet. We are encouraged to find that their capital costs ($209 500 haÀ1. see legend to Fig. (iii) the carbohydrate from the algae and the glycerol and other water soluble products are digested anaerobically when all the phosphate will be recycled. Their energy costs are about 15% of ours. although not entirely. which could have a market as supplements for low protein animal feeds such as corn meal (15% protein). A detailed costing was prepared for a pond/raceway type system. since there is considerable variance in the estimates for several major individual items between the two budgets. a power station) or an isolated facility. in large part. 94 gives a costing for a tubular bioreactor and ref.117 Although the capital costs were specified. however. An alternative calculation may be made pro rata from the price of soya This journal is ª The Royal Society of Chemistry 2010 . (ii) all of the non-lipid cell debris (plus the glycerol and other water soluble products from the transesterification process) is put to anaerobic digestion. with the production of methane (used to generate energy – in the process the nitrogen and phosphate are recycled). thus given a protein content we can derive an objective estimate of price. 3. The carbohydrates in the residual biomass could be used for ethanol fermentation. mid (35–45 ) and high (45–55 ) latitude bands using the production rates shown in Fig. Some of the numbers in the report in ref. converted from Canadian dollars using a Can/US exchange rate of 0. with the capital repayment costs removed. taken from the 3 : 2 protein to carbohydrate ratio used throughout this work. reflects the immaturity of the subject. The high protein content of the residual biomass could provide an excellent source of feed.119 These authors worked largely. whether the algal growth system is an adjunct to a CO2 source (i. 23. However. no significant change to the economic pattern seen in Fig. such as that described in ref. 15 incorporated the essence of this in the 1996 Report to the Pittsburgh Energy Technology Centre. There is. There is only a limited amount of information to draw upon to construct a costing algorithm. not enough information is present in the literature to date regarding the composition of individual sugars and concentration in the residual biomass as well as large unknowns about the recalcitrance of microalgal structural carbohydrates. about 10–15% of the total nitrogen (see Table 2). but only the small fraction of the nitrogen in nucleic acids and phospholipids. our estimate was $26 375. to leave it out of the costing algorithm but to return to it in our 580 | Energy Environ. 15 and 116. i. Ref. The DOE Aquatic Species Program commissioned a report (ref. Sci. In the economic analysis we consider three lipid levels (15. 2010. We have explored three scenarios surrounding the exploitation of the non-lipid fraction: (i) the carbohydrate and protein part of the cell debris is sold as animal feed ($60% protein. Similar uncertainties surround the fate of the residual biomass. For feed with 60% protein content a value of $750 tonneÀ1 is obtained.. 35 and 50% lipid as dry weight) and three latitudes: low (0–30 ). Animal feeding trials on algal preparations in general have been underway for some time. 24 if their labour costs are substituted into our economic analysis. ref.

c Scaled to lipid processed.41 $ kgÀ1 Biodiesel cost 1.kingsman. the carbohydrate and other water soluble products are processed by anaerobic digestion. although we suspect that this may be an underestimate. by the size of the culture area and the scale of processing. are assumed to be supplied as a mixture of di-ammonium phosphate and ammonia (costed at $325 tonneÀ1 and $300 tonneÀ1. 15 and 67.meal (protein content 45%. Whether algal biodiesel will be more valuable than ‘traditional’ biodiesel remains to be determined and will depend on the market when its fuel properties are better established. as methyl esters. kk Values for Europe. We have drawn a mean value of $916 Æ 73 tonneÀ1 from recent analyses by market specialistskk and have rounded this down to $900 tonneÀ1 – this approximates to $125/barrel. The required nutrients. d Scaled to tonnage digested. dw ¼ dry weight ASPECT OF PRODUCTION FACILITY UNITS Operating Parameters & Assumptions Areal production 28 g dw mÀ2 dÀ1 Annual tonnage produced 103 tonnes dw haÀ1 aÀ1 Lipid content 35% dw Protein : carbohydrate ratio 3 : 2 mass Lipid production 36 tonnes dw haÀ1 aÀ1 Bidiesel production (at 70% biolipid 25. the separation of the protein and carbohydrate fraction will have influence on the costing.07/kWha Diammonium phosphate (DAP)b 0 $ haÀ1 aÀ1 Ammoniab 2210 $ haÀ1 aÀ1 Transesterification – methanolc 1650 $ haÀ1 aÀ1 Transesterification – power requirement – 166 $ haÀ1 aÀ1 natural gasc Waste – energy value @ $0. In this example. these are rounded off values for $75/barrel and $100/ barrel. For the protein-only material the protein/price analysis is not regarded to be reliable as it exceeds the available data.2 tonnes dw haÀ1 aÀ1 production) Carbohydrate used for anaerobic 100% digestion Protein used for anaerobic digestion 0% Annual tonnage used for anaerobic 35 tonnes dw haÀ1 aÀ1 digestion Electricity yield from anaerobic digestion 139 000 MJ haÀ1 aÀ1 Growth area. Table 9 Basic structure of the spreadsheet costing model. as well as social attitudes towards higher plant biodiesel (see highlighted comment in the Gallagher report. b Scaled to biomass production. respectively) matched to the calculated nitrogen and phosphorous content for cells of low (15%). (ii) an allowance for operational downtime. medium (35%) and high (50%) lipid content (see Table 2). the latter is then converted to electricity assuming 35% efficiency. The costings are intended to be for a scale where they are no longer dependent of the size of the plant (i.. As a starting point we have used the above value. the nutrient cost is set to zero (this assumes 100% recovery). 2010.69 $ kgÀ1 Biodiesel cost 237 $ bblÀ1 Revenue from biodiesel (@ $900 tonneÀ1 22 700 $ haÀ1 aÀ1 Revenue from pure protein @ $900 36 200 $ haÀ1 aÀ1 tonneÀ1 Total revenue 58 900 $ haÀ1 aÀ1 Total expenditure 42 700 $ haÀ1 aÀ1 NET REVENUE 16 200 $ haÀ1 aÀ1 a Scaling of parameters: scaled to culture area. Asia and USA from ICIS pricing and for Europe from Kingsman (http://www. This assumption needs verification as it has a marked effect on some aspects of the costing. 3.07/kWha Harvest – power requirement – electricity 2660 $ haÀ1 aÀ1 @ $0. When all the non-lipid fraction is put to anaerobic digestion. We have conservatively used a rounded down value of the lower figure – $500 tonneÀ1. 554–590 | 581 .07/kWha Dewatering – power requirement – electricity 105 $ haÀ1 aÀ1 @ $0. median commodity value ca. no data on this separation step was found in the literature.88 and a barrel is taken as 159 litres. Furthermore. there is no further economy of scale). to the tonnage cell material produced.07 kWhÀ1 d À1120 $ haÀ1 aÀ1 Anaerobic digester operating costsd 2720 $ haÀ1 aÀ1 Captial costs @10% per annum 22 800 $ haÀ1 aÀ1 TOTAL COSTS 42 700 $ haÀ1 aÀ1 Product costs & revenues Biomass cost 0. Somewhat more critical is the price we assign to algal biodiesel. Anaerobic digestion is assumed to lose 25% of the calorific value of the feedstock during the production of methane. Sci. this gives a lower figure of $533 tonneÀ1. so their exact values are not critical. The biodiesel. a figure of $890 may be calculated pro rata from soya. the phosphate addition is set to zero and ammonia alone is added to satisfy the nitrogen requirement. All large numbers have been rounded off to 3 significant digits. where appropriate. $400 tonneÀ1). The figures are not too dissimilar from costings (inflation adjusted) used by ref. this has been rounded off to $900 for the purpose of calculation. the tonnage of lipid processed and the tonnage put to anaerobic digestion. The capital and operating costs of anaerobic digestion were supplied by a UK manufacturer. A round figure of 10% is taken for the combined loss from these three sources. but determined. plus two additional values: $550 tonneÀ1 and $700 tonneÀ1. and (iii) losses during harvesting. where appropriate. The spreadsheet (see Table 9) scales the costings. Losses on harvesting are presently not established. Section 1). In the scenario where the protein fraction is not digested but sold. with a 28 g mÀ2 dÀ1 (103 tonnes haÀ1 aÀ1) productivity and a lipid content of 35% of dry weight.e. There is a substantial literature surrounding the losses due to the release of organic material (a figure of 5% is used) and downtime is assumed to be 1 week per annum (a 2% loss). it is assumed to have a specific gravity of 0. nitrogen and phosphorus. To convert biodiesel from mass to volume units. as % site area 88% DAP costs per tonne biomass 0 $ tonneÀ1 NH3 costs per tonne biomass 21 $ tonneÀ1 Capital costs 41 800 $ haÀ1 aÀ1 Site prepa Culture systema 148 000 $ haÀ1 aÀ1 Engineeringa 22 000 $ haÀ1 aÀ1 Harvestb 3570 $ haÀ1 aÀ1 Extractionc 4560 $ haÀ1 aÀ1 Anaerobic digester @ $225 tonneÀ1 annumÀ1 8730 $ haÀ1 aÀ1 throughputd TOTAL CAPITAL COSTS 228 000 $ haÀ1 aÀ1 Running costs 4430 $ haÀ1 aÀ1 Laboura Growth – power requirement – electricity 7020 $ haÀ1 aÀ1 @ $0. shown for one example: a low latitude situation. There are three losses that need to be taken into consideration: (i) the production of extracellular dissolved organic material during growth. The model assumes that the cell’s protein : carbohydrate ratio is 3 : 2 and does not vary with lipid content. is sold at $900 tonneÀ1. the protein is separated from the carbohydrate and sold at $900 tonneÀ1 as high-grade animal feed. This journal is ª The Royal Society of Chemistry 2010 Energy Environ. It’s important to note that these values are only used as starting values for scenario analysis.

554–590 This journal is ª The Royal Society of Chemistry 2010 . red 50%. animal feed at either $500 tonneÀ1 (as low grade protein – dark blue bars) or at $900 tonneÀ1 (as high grade protein – pale blue bars). The calculation assumes biodiesel to have a commodity value of $900 tonneÀ1 (ca. A.Fig. The value the separate products. C. The details of the model are given in Table 9 and the text. Sci. $125 bblÀ1). B. biodiesel at $900 tonneÀ1. 24 Results of a spreadsheet model of costings and economics for the production of biodiesel and associated product streams. Lipid levels: blue 15%. 2010.. The net revenue calculation for anaerobic digestion involves the revenue gain from electricity production and the recycling of nitrogen (where it occurs) and phosphate minus the operating and capital costs of the anaerobic digestion plant. Net revenue. 582 | Energy Environ. 3. green 35%. The cost of biomass ($ tonneÀ1) and biodiesel ($ bblÀ1) assuming them to be the sole marketed product.

Sci. the algae are presumed not to enter nutrient limitation. although it certainly would be in the plant design. becomes uncertain (see Fig. a more attractive proposition. At liquid CO2 prices of $10 tonneÀ1 the pattern in Fig. gains from high lipid production only appear at biodiesel prices above $125 bblÀ1. the price determined from a recent study in ref. At $50 tonneÀ1. However at 50% lipid levels. is not a net source of revenue (Fig. The digester is assumed to enable 100% recycling of the nitrogen and phosphate in the feedstock for use in the culture media. even allowing for savings arising from the recycling of energy and nutrients.Fig. 24 remains much the same. By far the majority of algal ‘‘farms’’ to date have focused on high value products. have the potential to be very valuable. The analysis makes the point that the co-products. 6. 15. 25. The analyses are not particularly sensitive to lowering of oil prices – an analysis for $350 tonneÀ1 (nominally $50 bblÀ1) is much the same as the analysis for $550 tonneÀ1. 6). 121 for carbon capture and sequestration. 25 profitable on the costings used. 25 A matrix of the outcome of analyses of economic Scenarios 1 and 3 for the net revenue resulting from various commodity prices for the algal products. A summary of a matrix analysis for Scenarios 1 and 3 is shown in Fig. notably protein. However. 24B).. it this respect it may be providing optimistic estimates. A general trend of reducing revenue with increasing lipid content is apparent. On the other side of the coin. the assumption in the productivity model that sufficiently high growth rates can be sustained and only light limits growth. the sense exists that there is potential to improve upon present yields. where a considerable proportion of the energy yield has to be used to maintain the temperature of the digester. Potential gains in productivity could arise from modifications of the cell’s light capturing apparatus (see Section 4. The costs of anaerobic digestion come from temperate latitudes. so Energy Environ. Perhaps the most important finding is that the simple aim to increase lipid yields using high lipid containing algae may not necessarily be a sound economic strategy if the biochemical and other losses associated with lipid and biodiesel production are taken into consideration. Large uncertainties surround the costing of the plant – notably the harvesting and subsequent treatment of the biomass and the eventual market values of the various biomass components.2 Analysis of scenarios An illustration of the three end-product management scenarios is given in Fig. and for the protein-only scenario (Scenario 3) above values of $600 tonneÀ1. This may make the anaerobic digestion of protein. 2010. positive economic solutions can be found if the value of the protein + carbohydrate product (Scenario 1) is above $350 tonneÀ1. There is no doubt that our analysis can be improved upon and that there are uncertainties associated with many of the numbers used in the calculations. one may expect these circumstances to be very different at low latitudes. a rise of the same scale to from $100 to $125 bblÀ1 would make all the scenarios in Fig. This would be essential if the intention were for biodiesel to be the sole This journal is ª The Royal Society of Chemistry 2010 commodity. It is appropriate at this point to recognise that no costing has been made for CO2 supply. All of these assumptions need confirmation. We have chosen not to make allowance for these potential improvements. The present model assumes that light alone limits production. Anaerobic digestion (Scenario 2). profitable scenarios were only found at the higher price levels. waste heat from the generators is not put to any specific use in our analysis. This was also the earlier conclusion in ref. 554–590 | 583 . There is active ongoing research and this is one area where one can anticipate substantial advances in the not too distant future. at $100 tonneÀ1 profitable scenarios appear only with biodiesel prices of $125 and above. Whether the alternative of fermenting the carbohydrate and glycerol to ethanol offers better economic rewards would be worth exploring. 3.5). Given a value of $125 bblÀ1 for biodiesel. 24A. Furthermore. Uncertainties over the estimated areal production rates will condition the reliability of our economic analysis. along with carbohydrate. only at a lipid content of 50% of the cell’s dry weight does the revenue of biodiesel exceed that from selling the algal proteins.

$ Can/$ US ¼ 0.28 Biomass costs Assumed productivity $ tonneÀ1 g dw/mÀ2 dÀ1 % dw — — — 50 50 Not given Not given Not given 30 30 30 40 Not given 25 15 15 25 50 15–50 — — 5900 — — — — — 470 — — 370 — 600 — 2000–15 000 — 2140 — — — — — — 6100 4700–6900 30 400 — — — — — — — 110–360 — — — — — — 360–650 — — 241 148 — — — — — — — — 1600 [224] — — — — — — — — — — — — 1 6800 350–70 000 (1 4600 Æ 8200) — — — — — — PBR RW Hybrid PBR 20 3. it is assumed to have a specific gravity of 0.88 and a barrel is taken as 159 litres. To convert biodiesel from mass to volume units.7–14 15.3 9. (2007)123 Not specified Alabi et al.2) 30 60 Not given 20 16–20 27 72 35 19–60 2. 122. Sci.8 and V/$ US ¼ 1. (2004)94 Phaeodactylum Moheimani (2005)103 Dunaliella Pleurochrysis van Harmelen & Oonk (2006)122 Not specified Chisti (2007)4 Not specified Not specified Huntley & Redalje (2007)16 Not specified Carlsson et al. the currency conversions used are: $ Aus/$ US ¼ 0. 2010.Table 10 A comparison of published costings for algal biomass and biodiesel production.4 Æ 8.81.2–30 (14.. The estimates have been adjusted to 2007 prices.4 10 25 50 18–37 Assumed lipid content $ tonneÀ1 [$ bblÀ1] RW — — — 490 [69] 300 [42] — — — 1200 [168] — 2050 [287] — — — — 7500 [1050] 2250 [315] 750 [105] — Hybrid — — — — — — — — — — — 280–910 [39–127] — — — — — — 900–3500 [126–490] Biodiesel costs 584 | Energy Environ. 3. (2009)119 Not specified Not specified Pienkos & Darzins (2009)95 Not specified Not specified Not specified This journal is ª The Royal Society of Chemistry 2010 Present account Not specified . We have only taken the median value from ref. 554–590 Source Organism Borowitzka (1992)117 Not specified Various Mean (+StDev) Benemann & Oswald (1996)15 Not specified Not specified Molina Grima et al.

the broad patterns in the economics are probably correct.. we would see in many respects that producing models of algal production is a more tractable problem than many of the others above and the potential exists to produce robust models in the not too distant future. likewise contains high values for manpower and harvesting. 119 also stands out as high-cost estimates. the yields are reduced to two-thirds from about 30–40 g dry weight mÀ2 dÀ1 (100–140 tonnes haÀ1 aÀ1) to 20–25 g dry weight mÀ2 dÀ1 (67–93 tonnes haÀ1 aÀ1) then we find it difficult to produce economic scenarios. At first sight they seem disturbingly disparate: estimates for biodiesel costs range for $280–$7500 tonneÀ1 ($39–$1050 bblÀ1) and biomass from $110– $30 400 tonneÀ1. as a percentage of total costs. in our analysis in Section 6 we found that.1 Can the production of algal biomass (or biolipid) be made profitable? The evidence from our analysis is a conditioned yes. We derive a figure in the region of 10% in the present analysis. The costings in ref.the incentive to undertake expensive R & D to increase yields has been low. potentially setting a limit to the scale of production. as the properties of the alga used. the spread is still large but reduced to $110–$600 tonneÀ1 for biomass and $280–$2050 tonneÀ1 ($39–$315 bblÀ1) for biodiesel. 119. non-viable. 94 derives from an advanced PBR system. to market other biomass products. of course. we are only able to find profitable outcomes if all the major biochemical products are processed and marketed. 123 are based on an extremely cautious assumption of growth yields (2. In particular. A third area of uncertainty deals with the future market prices for the various commodities – notably the value and acceptability of algal protein as an animal feed and. and on an industrial Energy Environ. in which it was concluded that the ‘‘fuel only’’ option was not economically plausible – other revenue sources were needed to bring the system into profit. the market price of biodiesel. i. Our finding is in agreement with ref. but a greater (15–30%) loss at high latitudes. We are unable to find economic solutions for the marketing of biodiesel alone and the associated recycling of the nutrients and energy in the non-lipid fractions by anaerobic This journal is ª The Royal Society of Chemistry 2010 digestion. If legislation for minimum additions of biodiesel to fuels persists and the ecological concerns over higher plant fuels continues or rises.7–14 g dry weight mÀ2 dÀ1). Thus. 7. First. whether it has to be used for primary separation (which seems unlikely) or final concentration. We find it difficult to see how systems can be run in profit with biomass yields below 20 g dry weight mÀ2 dÀ1. Although predicting yields is a complex matter. 117 analysis implies a similar figure: 15–25% of the capital costs and 20% of the operating costs were associated with harvesting. but in the uncertainty over what procedures will be used. we have not been able to obtain costings for anaerobic digestion at low latitudes.e. As discussed in Section 6. will be used. they made their analysis for the latitude of British Columbia ($50 N). There are broadly four areas of uncertainty in the economic analysis. and the analysis in ref. Estimates of harvesting costs (capital and operating costs). although it would be unrealistic to expect the exact values to be. Sci. Part of the reason for the high costs in the latter study are the conservative assumed yield rates (15 to 20 g dry weight mÀ2 dÀ1) used in the analysis. intended for a high value product. in addition to biolipid. 554–590 | 585 . 6.2 What R & D is needed to achieve these aims? A number of reports have considered the R & D required to produce algal biomass economically. given the most favourable form of culture – a photobioreactor/raceway hybrid – we can envisage a number of scenarios that would appear to have the potential to yield net profit.3 Comparison with other economic analyses We have compared the costings published in the literature. The analysis in ref. over which there is reasonable consistency. 7 Prospects and research needs In summing up the review we explore the answers to two questions that arose through the course of the review: (1) Can the production of algal biomass (or biolipid) be made profitable? (2) What R & D is needed to achieve these aims? 7. If. 122. versions of the present report and the worst case scenario of the analysis in ref. but also in Borowitzka’s study an apparently high operational cost. will determine the strategy that can be used for harvesting. 103. 15 gave range of 20–25%. This has implications. The fourth major uncertainty lies in the prediction of biomass yields. its nutritional and physiological status. First. whether or not and to what extent centrifugation. If the first option is adopted. A second major uncertainty relates to the cost of harvesting. 103 gave a range of 40–50% for the harvest and processing costs for the calcium carbonate-containing coccolithophorid Pleurochrysis carterae and 63% for Dunaliella salina. yields have a pronounced effect upon the economics. with prices for biodiesel up to $1400 tonneÀ1 ($200/barrel). similar to the estimate of 12% in ref. effect on strain selection. The estimate in ref. Table 10 gives a collation of published costings.e. the market for protein will control the overall scale of production. where biomass yields would around half those from latitudes of 0–30 . notably protein as animal feed. Doubling the harvesting costs in our analysis gives rise to a 10–15% fall in revenue of the more profitable scenarios at low latitudes. 95. i. Further. which again is high. the numbers must also be considered in context – the high estimate reported in ref. Ref. Despite the uncertainties. vary considerably in different economic analyses. The careful analysis in ref. which seems out of line with other costings. This investment will need to be made to increase sustained algal biomass production rates if we are to use algae for relatively low value products such as biodiesel and animal feed. The analysis in ref. Much of this variability derives not from the uncertainty in the costings themselves. for example. If we consider the remaining analyses and disregard the high cost. This could extend the economic viability. 117 contains his own estimate and summarises earlier work – the average of these estimates in the region $15 000 tonneÀ1. This is probably the most complex of the problems. then this may inflate the value and so price of algal biodiesel. if not overriding. however. 3. Harvesting costs will have a major. 2010. which has high capital and operating costs.

may not be an option as a primary form of separation on cost grounds. In ref. as yet.4). This maximum yield.3). simple first order empirical models based on energetics. India. 22. 15 it was noted that the type of strain needed would be as ‘‘as common as hen’s teeth’’ in Nature. South-East Asia and Australia would however be well placed to develop such technologies. Russia and Canada. the current status of filtration and micro-straining technology does not allow for a viable option for harvesting algae on a large scale. The losses are principally due to wastage of the energy of the collected photons at high photon flux rates. Commonly used. but there may also be a secondary effect of light mediated through temperature.5. Fundamental physiological models of algal growth exist. they used a mean annual temperature of 15  C as a criterion. One matter that needs urgent consideration is the apparent irradiance threshold (see Fig. Furthermore. 3. (i) Optimising yields. but by slowing down the photochemical reaction by reducing the photon capturing capability of the cell. but the compilation came from very disparate studies and in many cases required data conversions and any pattern may have been lost or concealed within the resultant noise. in the field of mass production of algae. The present review reaffirms this. involving a number of positive and negative feedbacks (see Section 4. There has been work done on this and progress made. as other issues that surround the use of GMOs. as soon as the economics are extended beyond the production of lipids and biodiesel. This may well be the case. agglutination or co-precipitation in combination with a centrifugation step to harvest cells.5(i) and its probable resolution lies not in increasing the rates of the dark reaction. 50 and 125). there is no fundamental barrier to achieving the theoretical yields. have set their face against going down the latter route. This is particularly the case when products other than lipids are part of the overall economic equation (see Section 6 and Fig. Actual yields fall short of this. 122 a latitude boundary of 35 was suggested.4(ii)). will need to be debated.3. carbohydrates and proteins) was analysed in Fig. these models will need dedicated studies on microalgae in order to calibrate them.1). Sci. and geographically limit it in the US and China. Following on from the above. however finding solutions that are economically viable present severe practical challenges. There is a pressing need to establish whether or not this apparent irradiance threshold is a general phenomenon and. if it is we need to gain a better understanding of its physiological basis. advancing our understanding of harvesting and processing strategies and resolving the problems of scaling up. Lipid content by itself would seem of limited value. This brings to the fore the need to distinguish between high lipid containing algae and high lipid yielding algae. (ii) Advancing our understanding of strategies for harvesting and processing of algal biomass. The point has been made on a number of occasions that centrifugation. This. as a major area of uncertainty that has major economic implications (as discussed in section 5. the Middle East. It is very unlikely to come from screening of natural species but rather through genetic engineering.. In relation to this. These could be adapted to microalgae.scale. One is left with some form of flocculation. This may be subdivided into two broad problems – increasing production rates and maximising the economics of product yields. is constrained by stoichiometry and thermodynamics and. As far as we can determine. advances in centrifugation engineering may improve the economics.3(ii)). a pressing matter is to determine whether the apparent negative relationship between lipid content and growth rate exists (see Fig. one could use these models as powerful predictive tools.15 The list of R & D needs is very long and there is no need to detail these at length. In ref. may be considered to be immovable. The problem was discussed at length in Section 4. sensitive to the negative public reaction towards genetically modified organisms (GMOs). such as that employed in Section 4. We conclude that this cannot 586 | Energy Environ. 3 and no pattern was evident. Network models for the flows of material during metabolism have been developed for higher plants (see ref. the value and the dynamics of the quantitative distribution of the other major biochemicals within the cell become a major issue. for all practical purposes. cannot incorporate these feedbacks in any explicit way and thus can only be considered as first order solutions. Again. This derives mainly from a mismatch between the processing rates of the photochemical and enzymatic reactions. In a growing microalgal culture there is a complex of interactions between the organism and the physical and chemical environments. The aim here is to give emphasis to the R & D requirements that this review has indicated to be of greatest importance and urgency: optimising yields. 7 and the associated discussion in Section 2. Some major players in the field. Once they are available. To provide some This journal is ª The Royal Society of Chemistry 2010 . They will be needed to optimise production rates – further they have the potential to serve as an exploratory tool – to determine the environmental criteria necessary for economic production. However. often being in the region of one third to one tenth of the theoretical maximum (see Section 4. Many of the previous analyses of R & D needs have pointed to the requirement to isolate or develop high lipid producing algae. Most of Africa. technological advances in membrane and systems engineering could change this supposition. Such latitudinal boundaries would exclude yearround production in the EU. we point out. and particularly harvesting. A collation of the reported proportions of the major biochemical fractions (lipids. Reviews and reports invariably point to processing. In Section 3 we developed the broad basis for the theoretical photosynthetic yields – a figure in the region of 10% of the energy in incident irradiation incorporated into organic material is a widely accepted value.124 but do not appear to be extensively used. there seems limited capability to do this.5(iii). 2010. by some intrusive procedure – essentially locking the cell into the high light adapted state. as they would have little to no competitive capability. if it has to be achieved at the expense of growth rate. 554–590 be solely attributable to the compensation irradiance. This will require modifying the control of the cell’s light capturing apparatus. Similarly. It may set an upper latitude boundary for yearround production. although conceptually and operationally simple. A major issue is whether this could be achieved by classical plant breeding techniques – induced mutations (so called ‘‘accelerated evolution’’ techniques) or by direct manipulation of the genome. and text in Section 4. However. 24). the strong species-dependent nature of the filtration process makes it difficult to draw conclusions about the general applicability of this process. Central and South America.

This returns us again to the problem of the recycling of phosphate within the overall scheme of production and the successful. (ii) the energetic budget and whether or not the net energy yield improves with the increasing ambient temperature at lower latitudes. bioethanol after fermentation of the structural sugars. current published carbohydrate information does not allow predictions of their potential yield. lipid and carbohydrate fractions from one another. the cost. (iii) Resolving the problems of scaling up. The engineering and energy costs for pumping could be considerable and almost certainly one would need to resort to recycling water to some extent. At present rates of exploitation the global reserves are estimated to have a lifespan no more than 50–100 years. We are. nitrogen and phosphorus in particular. Of the three major nutrients. and. Work on this was recently reviewed in ref. and thereby carbon neutral. Whereas we have extensive knowledge of the application of anaerobic digestion to human and animal waste and a growing knowledge of the treatment of domestic waste. is a by-product of the Haber–Bosch process (used for ammonia synthesis) and its release into the atmosphere will need to be incorporated into any life cycle analysis. in addition to land and sunlight. Neither is likely to be a low cost solution. practicality and utility of separating the protein. rather than separating and processing the individual biochemical fractions. significant quantities of water and nutrients. local water supplies are unlikely to be adequate and so water (for a number of reasons most probably seawater) will need to be pumped onto the culturing site and after use disposed of in some manner. There is experience of these matters from the existing production plants. In the analysis in Section 6. is water. However. pathogens such as viruses if not removed will be recycled. In contrast to nitrogen. carbohydrate was relegated to a low value commodity.. 2010. Once a concentrated slurry of cells has been produced we have a number of processing options. 115. however. It may be possible to achieve this by active aeration relying upon the ambient concentration in air. research is needed to determine whether the bulk carbohydrate fraction or a sub-fraction can be put to better use than simply recouping a fraction of its energy by anaerobic digestion. Biological contaminants. There remains the question whether. not without experience of applying anaerobic digestion to algal material. social and economic as well as scientific. at the minimum. required for algal mass culture. physiology and culture conditions. more specialised biochemical. As discussed in Section 4. were considered in Section 6 (see Fig. as this was undertaken as part of the high oxidation rate ponds used in some of the US west coast sewage treatment plants. perhaps more problematic. not surprisingly. for example material added to induce flocculation will be present or will have to be removed from the spent medium. there is value in subjecting algal biomass to some form of thermal upgrading for producing biofuels. nitrous oxide.g. There are a number of potential ‘‘show stoppers’’ to sustained production on this scale. requires. Recycling of the spent culture medium is embedded in the conceptual scheme in ref. This. Three scenarios. although this would be costly or it may be necessary to actively separate the CO2 from the atmosphere by liquefaction and add pure CO2 to the culture. the spent culture medium will contain soluble organic products released during algal growth. To make a significant contribution to global fuel production one needs to consider the question of sustainable production approaching the near gigatonne scale. carbon dioxide has to be added to the culture in some way. a powerful greenhouse gas. and (iii) the fraction that remains undigested over some economic time scale and whether it has value as a fertiliser or soil conditioner. However even if the energy were derived from within the algal production facility. Algal mass culture. not surprisingly.4(iv). Major questions surround the application of anaerobic digestion to the processing of ‘‘waste’’ algal debris. Energy Environ. in order to achieve rapidly growing dense cultures. and the further separation of valuable. 24). 554–590 | 587 . a great deal more will be required before we can establish the practicalities and their relative economics. This may call for further treatment e. There are two levels of scaling up: (i) from the laboratory to the pilot plant/modest production plant scale.126 One-off use of phosphate on a gigatonne scale of algal lipid production would add significantly to the present demand and shorten the lifespan of the global phosphorus reserves. Compositional analysis of the algal biomass will determine whether the carbohydrate fraction can be used to generate a second biofuels stream. e. it can be generated from atmospheric nitrogen. use of anaerobic digestion to achieve this. 3. Similarly any residual additives. competitors and predators. The third potential ‘‘show stopper’’. These raise major R&D questions. A second possible ‘‘show stopper’’ is the availability and delivery of significant quantities of CO2. 95. by comparison we have a very limited knowledge of the digestion of microalgal debris. as the natural exchange across the atmosphere is too slow. Sci. As soon as one anticipates production plants of considerable scales. The second brings along This journal is ª The Royal Society of Chemistry 2010 a number of special considerations. or otherwise. nutraceutical and potential pharmaceutical products. which involved overall various ways of handling the major biochemicals. however. given energy. We need insight on a number of matters surrounding anaerobic digestion: (i) the speed and completeness with which nitrogen (presumably as ammonia) and particularly phosphate are released and therefore recycled. sterilisation of the recycled water with inevitable cost implications. The first is essentially scaling up from gram to tonnage production and is associated with the R&D needs outlined above. Recycling of used water brings along a number of problems. A first possible ‘‘show stopper’’ is the availability of the nutrients.g. (ii) from the pilot plant scale to a scale that would make a significant and sustainable contribution to global liquid hydrocarbon fuel production. these will accumulate and may have a positive or negative effect upon the growth rate of subsequent cultures.strategic basis we need a much more detailed understanding of the surface properties of the cell and how this varies with species. supplies of phosphate would need to come from very finite reserves. How easy it would be to transfer this knowledge to the residual cell material from mass algal culture needs to be explored.g. e. nitrogen might be argued not to be a problem as. it will call for a major research effort. brings along a host of problems: political. As we start from a position of very little existing knowledge in the case of microalgae. three of them merit early consideration and research. however without some basic understanding we will be committed to continue to fumble our way through the problem by trial and error.

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