J Appl Phycol (2009) 21:493–507 DOI 10.


Lipid productivity as a key characteristic for choosing algal species for biodiesel production
Melinda J. Griffiths & Susan T. L. Harrison

Received: 31 July 2008 / Revised and accepted: 12 November 2008 / Published online: 6 January 2009 # Springer Science + Business Media B.V. 2008

Abstract Microalgae are a promising alternative source of lipid for biodiesel production. One of the most important decisions is the choice of species to use. High lipid productivity is a key desirable characteristic of a species for biodiesel production. This paper reviews information available in the literature on microalgal growth rates, lipid content and lipid productivities for 55 species of microalgae, including 17 Chlorophyta, 11 Bacillariophyta and five Cyanobacteria as well as other taxa. The data available in the literature are far from complete and rigorous comparison across experiments carried out under different conditions is not possible. However, the collated information provides a framework for decision-making and a starting point for further investigation of species selection. Shortcomings in the current dataset are highlighted. The importance of lipid productivity as a selection parameter over lipid content and growth rate individually is demonstrated. Keywords Algal biodiesel . Lipid productivity . Species selection

Introduction Biodiesel is currently receiving much attention due to its potential as a sustainable and environmentally friendly
This paper was presented at the 3rd Congress of the International Society for Applied Phycology, Galway. M. J. Griffiths : S. T. L. Harrison (*) Centre for Bioprocess Engineering Research, University of Cape Town, Rondebosch, 7701 Cape Town, South Africa e-mail: sue.harrison@uct.ac.za

alternative to petrodiesel. It is generally made by transesterification of vegetable oil, primarily from rapeseed, soybean, sunflower, or palm (Ma and Hanna 1999; Xu et al. 2006). While biodiesel is a desirable product, the significant economic and environmental impact of using agricultural crops, especially food crops, as a feedstock for biofuels raises crucial sustainability issues. For example, the increased demand for these crops will affect their price in the food market, place additional demand on the often strained agricultural system and impose a negative environmental impact through the additional energy requirements and eutrophication caused by intensive agricultural processes (Chisti 2008). Microalgae are a promising alternative source of vegetable oil. Due to their simple cellular structure, algae have higher rates of biomass and oil production than conventional crops (Becker 1994). Some species of algae produce large quantities of vegetable oil as a storage product, regularly achieving 50% to 60% dry weight as lipid (Sheehan et al. 1998). Hence, algae have been claimed to be up to 20 times more productive per unit area than the best oil-seed crop (Chisti 2008). Other advantages of algae are that they can be grown in marginal areas such as on arid land or potentially in the ocean. Many species tolerate brackish or saline waters (Tsukahara and Sawayama 2005). These reduce competition with food crops for agricultural land and fresh water. Production of biodiesel from algae is technically, but not yet economically, feasible (Chisti 2008). The major economic bottleneck cited in the literature is algal productivity, followed by labour and harvesting costs (Borowitzka 1992). Laboratory yields are reportedly rarely reached in large-scale culture, due to issues such as contamination, evaporation, flooding and lack of control over temperature and light provision in open ponds, as well as difficulties

The first step in developing an algal process is to choose the algal species. A single algal species is unlikely to excel in all categories. Growth over range of seasons and ambient weather conditions Greater potential for CO2 sequestration and use of waste CO2 Allows cheaper pumping and mixing methods to be used Potential growth in polluted water and on flue gases containing high CO2. those with slower growth rates could potentially be maintained in a closed photobioreactor to facilitate accumulation of higher lipid contents. available resources and choice of culture system influence species choice. Examples include large cell size. NOx and SOx Reduces autoinhibition of growth at high biomass densities . Developing a framework to guide choice of appropriate algal species A variety of desirable characteristics reported for large-scale algal culture are summarised in Table 1. productive strains. The Aquatic Species Programme (Sheehan et al. High growth rate also reduces contamination risk owing to out-competition of slower growers in planktonic. the number of strains commonly exploited in algal biotechnology remains few (Grobbelaar 2000). (1995) Grobbelaar (2000) Competitive advantage over competing species. An often-overlooked criteria when selecting species is ease of harvesting. Some algae are most productive at high temperatures and bright light. colonial or filamentous morphology Wide tolerance of environmental conditions CO2 tolerance and uptake Tolerance of shear force Tolerance of contaminants No excretion of autoinhibitors Advantages prioritisation is required. (Note: use of metabolic energy to generate product usually leads to slower growth) Reduces contamination and predation. contributes to both economic success and environmental sustainability. nutraceuticals or a nutrient-rich biomass. For example. Choosing a species well suited to the biorefinery approach. More recently. optimised for the local climatic conditions is of fundamental importance to the success of any algal mass culture and particularly for low-value products such as biodiesel. Can be difficult to maintain conditions) Reduces harvesting and downstream processing costs Less control of culture conditions required. (Note: Limited number of species can grow in extreme environments. 1998). Harvesting of algal biomass is a significant capital and operating cost in any algal process.000 species and screened several of these for lipid production. the quality of the available water supply and the rate of evaporation expected determine the salinity tolerance required of the algae. Rigorous selection is challenging owing to the large number of microalgal species available.494 J Appl Phycol (2009) 21:493–507 with fouling limiting light intensity and oxygen build-up in closed photobioreactors (Pulz 2001. High biomass density increases yield per harvest volume and decreases cost. but a final recommendation of species is not provided. Selection of fast-growing. hence it is desirable to select an alga with properties that simplify harvesting. hence Table 1 Desirable characteristics of algae for mass culture Characteristic Rapid growth rate High product content Growth in extreme environment Large cell size. Lee 2001). 1998) focussed on the isolation of high lipid content algae for growth in open ponds supplemented with CO2 from coal-fired power stations. Pulz and Gross (2004) observed that: “successful algal biotechnology mainly depends on choosing the right alga with relevant properties for specific culture conditions and products”. Rodolfi et al. high specific gravity compared to the medium and reliable Reference Borowitzka (1992) Borowitzka (1992) Borowitzka (1992) Borowitzka (1992) Borowitzka (1992) Grobbelaar (2000) Grobbelaar (2000) Borowitzka (1992) Zeiler et al. Certain algal species cannot be grown reliably outdoors as they are quickly out-competed by faster growing algae. Harvesting unicellular algae from solution remains a major challenge and the dilute biomass produced further aggravates the need for an integrated approach to minimising consumption of water and energy as well as downstream processing cost (Benemann et al. A high content of the desired product increases the process yield coefficient and reduces the cost of extraction and purification per unit product (Borowitzka 1992). They isolated over 3. reduces culture area required Higher value of biomass. Fast growth encourages high biomass productivity. while growth of others is retarded by full sunlight (Sheehan et al. However. for example producing valuable co-products such as fine chemicals. Environmental conditions. Little consensus is reported between research groups on the algal species most suitable for biodiesel production. Further. continuous culture systems. the limited characterisation of these algae and their varying sets of characteristics. (2008) screened species for high lipid productivity and found the marine Nannochloropsis and Tetreselmis to be particularly promising. 1977).

g. it was discarded. Micractinium. Pseudokirchneriella subcapitata. All microalgal species currently grown on a large scale. Data were collated at species level wherever available. In a few cases.and mixotrophic conditions were sparse. Biddulphia (Odontella) aurita. while vegetable oils currently used for biodiesel are mainly C16 and C18 (Harrington 1986)). degree of saturation and proportion of total lipid made up by triglycerides. Nutrient deficient: Specified nutrient was completely removed from the culture medium or reduced below stoichiometric requirements for growth.g. or maintaining a batch culture until nutrient levels in the culture medium have been shown to be severely depleted. using a very limited number of species. For the purposes of this review. The proportion of various lipid classes (particularly triglycerides) varies widely with environmental conditions (Rodolfi et al. For the purposes of this review. 2002). The majority of lipid-producing algal species have a similar lipid profile. 2008). the following definitions are used: & & Nutrient replete: Stoichiometrically balanced nutrient conditions were assumed where no evidence of nutrient reduction or depletion in the medium was provided. 1977)) are developed. however. hydrocarbons produced by Botryococcus braunii have a chain length of greater than C30 (Banerjee et al. & & Metabolic mode: photoautotrophic. These influence the quality of biodiesel produced. insufficient quantitative information is available in the literature to be able to compare more than a handful of the best-known species on these criteria. making it difficult to compare algal species across experimental conditions (Molina Grima et al. design and scale are reported under various conditions of nutrient supply. A wide range of reactor configuration. Sheehan et al. 1998).J Appl Phycol (2009) 21:493–507 495 autoflocculation (Borowitzka 1997). typically nitrogen or silicon deficiency. outdoor pond or outdoor photobioreactor This review is restricted to photoautotrophic conditions as the data for hetero. spanning a variety of algal species used across a broad range of purposes. is well known to enhance the lipid content of algae. Ochromonas danica. lipid contents and lipid productivities were gathered from a broad range of literature. These properties critically influence the process economics for low value products until such time as innovative. nitrogen deficient or silicon deficient Nutrient deficiency. e. These include fuel production. Nutrient levels have been reduced by differing amounts across studies reported. either by changing the medium. The only two characteristics relevant to biodiesel production that have been measured quantitatively for a wide variety of species are growth rate and lipid content. the references used described the organisms to genus level only. Botryococcus braunii is a notable exception with extremely long chain lengths (Banerjee et al. and species where the algal lipids produced were unsuitable for biodiesel (e. chain length. critical review of the information currently available in the open literature on the lipid productivity of microalgal species is presented to facilitate decision-making on species selection for biodiesel production. Roessler 1990). Units of quantification Typically. An additional algal characteristic for biodiesel production is the suitability of lipids for biodiesel in terms of the type and amount produced by an algal species. the data gathered was sorted into the following subcategories: & Culture method: laboratory. or considered in the context of lipid or biodiesel production were initially recorded. as well as tolerance to a wide range of culture parameters such as temperature and salinity. Further. calorific value as a food or feed and production of specialty oils and chemicals. 1998) and Cylindrotheca (Chisti 2007. Methods of data collation and analysis Gathering data Growth rates. the paper seeks to highlight gaps in current knowledge. generally equivalent to vegetable oil from land plants suitable for biodiesel production (Xu et al. heterotrophic or mixotrophic Nutrient availability: nutrient replete. Ostreococcus tauri. In this paper.g. Sheehan et al. Where recorded in picograms lipid per cell in the absence of cell weight. hence. Emiliania huxleyi. Lipid content has been reported under both nutrient-replete and deficient growth conditions (Shifrin and Chisholm 1981. Biomass productivity was usually reported on a volumetric basis in units of grams per litre per day and on a basis of surface area in units of grams per square metre per day. Chlorococcum. while growth rates were reported as doubling time (Td) . cost-effective methods of harvesting dilute microalgal biomass consisting of cells less than 20 μm in diameter (too small for low-cost straining or filtration (Benemann et al. Amphora (De la Pena 2007. e. The resultant list was refined by excluding species where reliable data for biomass productivity and lipid content could not be found (e. Other characteristics critical to success of large-scale production include resistance to contamination. 1994). 2006).g. lipid content was reported as percentage dry weight (% dw). 2002). Synechocystis aquatilis).

with interconversion as follows: QV ¼ QA D=1. grams per litre per day). Data presented as a specific growth rate in the absence of biomass concentration. Nutrient limitation. Figure 1 shows the average laboratory lipid content for green algae (Chlorophyta) and blue-green algae (Cyanobacteria) under nutrient-replete and nitrogen-deficient conditions. between 5% and 13%. This has resulted in algal species being re-classified. Petersen) Hibberd Monoraphidium minutum (Nägeli) Komárková-Legnerová Monoraphidium minutum (Nägeli) Komárková-Legnerová Porphyridium purpureum (Bory de Saint-Vincent) K. Lipid content (in % dw) is given for nutrient-replete. making collation of information confusing. Sheehan et al. volumetric biomass productivity (grams per litre per day) and biomass productivity on the basis of area (grams per square metre per day). μ is specific growth rate per day and X is biomass concentration in grams per litre. is well recognised to influence lipid content (Shifrin and Chisholm 1981. especially N and Si. Table 2 Current species names and their previous classification Current name Dunaliella salina (Dunal) Teodoresco Ettlia oleoabundans (S. C. QA is areal productivity in grams per metre squared per day. 1998). Biomass growth and productivities are given as Td.g. Hence. The latter are inter-converted according to Eq. all biomass productivities should be reported in standard units (e. Where appropriate data were available. Silicon deprivation is only relevant for diatoms (Bacillariophyta and some Ochrophyta). Lipid content Lipid content data were readily available and consistently reported in the literature. with an average of 8%. 000 ¼ mX where QV is volumetric productivity in grams per litre per day. for comparison purposes. Komárek Monodopsis subterranea (J. lipid productivity was calculated as the product of biomass productivity and lipid content.496 J Appl Phycol (2009) 21:493–507 or specific growth rate. with the exception of Chlorella sorokiniana which did not change. The two most common problems were: & & Data given as areal productivity in grams dry weight per square metre per day without reporting depth of the culture vessel. Lipid productivity was generally reported in milligrams per litre per day. only Oscillatoria showed an increase in lipid content with nitrogen deprivation. The overall average values for all species across each criterion are shown in the final row. The nutrient-replete lipid content for green algae ranges from 13% to 31% dw. Bold) J. D is depth in metres. Species names Algal taxonomy is evolving as molecular methods improve. Ideally. Chantanachat & H. For green algae. The average lipid content of 41% dw reported under nitrogen deprivation shows a twofold increase. Frequently insufficient information was provided for conversion. nitrogen (N)-deficient and silicon (Si)-deficient conditions.B. Td ¼ lnð2Þ m ð1Þ Analysis of algal species using laboratory data Data collected for 55 different species under laboratory conditions are presented in Table 3. the data in different units have been reported separately in Table 3. Lipid productivity (milligrams per litre per day) is presented in two columns: & & Average lipid productivity reported directly in the literature Lipid productivity calculated from laboratory biomass productivity in grams per litre per day and nutrientreplete lipid content Biomass productivity in continuous culture is determined as the product of specific growth rate (μ) and biomass concentration (X). Drew & Ross Selenastrum gracile Reinsch Previous names Dunaliella bardawil Neochloris oleoabundans Monodus subterraneus Ankistrodesmus minutissimus Selenastrum minutum Porphyridium cruentum Ankistrodesmus gracilis . 1. nitrogen deprivation was reported to increase lipid content. Species reported by a variety of names in the literature are summarised in Table 2. while the Cyanobacteria range is markedly lower. In the Cyanobacteria. with an average of 23%. and their currently accepted classification specified.

67 22 51 5 24 40 19 18 21 18 22 109 16 13 19 38 40 7 8 17 9 13 7 9 11 11 0. 63.27 38 30 77 52 38 48 63 82 Amphiprora hyalina Amphora Anabaena cylindrica Ankistrodesmus falcatus Chaetoceros calcitrans Chaetoceros muelleri Chlamydomonas applanata Chlamydomonas reinhardtii Chlorella emersonii Chlorella minutissima Chlorella protothecoides Chlorella pyrenoidosa Chlorella sorokiniana Chlorella vulgaris Crypthecodinium cohnii Cyclotella cryptica Cylindrotheca Dunaliella primolecta Dunaliella salina Dunaliella tertiolecta Ettlia oleoabundans Euglena gracilis Hymenomonas carterae Isochrysis galbana Monodopsis subterranea Monoraphidium minutum Nannochloris Nannochloropsis Nannochloropsis salina Navicula acceptata Navicula pelliculosa Navicula saprophila Nitzschia communis Nitzschia dissipata Nitzschia frustulum Nitzschia palea F M F F F F M M M S S S F F M M F F M/F M M F F F M M M M 34 27 14 10 18 42 35 14 29 13 52 30 41 46 35 45 51 3 33 2. 58. 61. 58. 56. 61. 5. 61. 74 5. 70 65 5. 36. 18. 45. 39. 39. 65 25.03 0. 54. 63 59 22. 16.16 0. 65 29 31 13 16 18 25 25 18 27 23 19 15 36 20 20 25 25 22 28 31 27 33 27 24 C C C C C C D O B Pr Pr Pr C Eg H H E C C E E B B B B B B B 48 497 . 62. 65. 70 15. 41. 65. 11. 60. 63 11. 47.11 45 26 97 28 0. 63. 9. 33. 17. 38.04 0. 15 36. 63 63 1. 67 3.46 0. 15. 64 56. 51. 61. 69 50. 65 6. 60. 39. 65 36. 15. 55. 38.07 37 % dw g L−1 day−1 N deficient Si deficient Nutrient replete Td (h) Nutrient replete g m−2 day−1 Nutrient replete Nutrient replete mg L−1 day−1 Literature Referencesc Calculated Nutrient replete mg L−1 day−1 Species Taxaa J Appl Phycol (2009) 21:493–507 10 20 24 8 160 B B Cy C O O C C M M F F M M F F 36. 63. biomass and lipid productivity for 55 microalgal species and genera reported in the literature Mediab Average from literature Nutrient replete % dw % dw 28 40 32 5 32 27 33 6 63 57 23 64 18 42 11 38 0. 36. 47. 65. 19. 65 63 6. 6. 40. 20. 35. 31. 68 8. 33. 66 26. 11. 63 17. 58. 36 36. 38. 63. 72 5. 32. 33. 17. 65.19 8 12 29 46 34 49 28 26 47 46 40 47 10 5 9 23 9 32 14 0. 61. 63 5. 61.Table 3 Average laboratory lipid content. 63. 44. 63. 65 15. 63 22. 47 6.46 14 41 21 136 164 12 0. 63 61 14. 63 5. 11. 63 21. 59 28. 17. 59.23 0. 23. 48. 67.03 8 10 36 11 0. 17. 63. 57.55 0.

64 Shehata and Kempner (1977). 65 34. 61. 65 11. 7. 67 Sorokin and Krauss (1961). 19 Cook (1966). 24 Ferguson et al. 22 Dempster and Sommerfield (1998). 51 Nagle and Lemke (1990). Pr Prasinophyta b Key to media: F fresh. 54. 29. 34 Ishida et al. (1991). 38. 30 Grobbelaar (2000). 57 Qiang et al. 65 5.12 0. (2001). 36 Johansen et al.21 0. (1984). (2003). 70 Taguchi et al. (1988). O Ochrophyta. (2008). 55 Piorreck et al. 63 46. 42 Maddux and Jones (1964). (2007). 13 Ceron-Garcia et al. 27 Goksan et al.23 25 20 0. 65 54. 53 Parrish and Wangersky (1987). 66 Siron et al. (2001). 56 Price et al.08 25 28 0. (2001). (2006) J Appl Phycol (2009) 21:493–507 . 33 Illman et al. 3 Apt and Behrens (1999). (1990). (2000). 61. (1997). 18 Constantopoulos and Bloch (1967). (2007). 62 Roessler (1990). 14 Chelf (1990). 63 15. 61 4. 24. 9 Bhaud et al. 54. 10 Bopp and Lettieri (2007). (1998). 63 Sheehan et al. 47 50 49 45 35 75 49 72 24 42 28 25 10 26 26 24 16 32 41 11 18 11 66 0. 59 Renaud et al. 73 Vieira Costa et al. 69 Suen et al. 68 Spoehr and Milner (1949).498 Table 3 (continued) Mediab Average from literature Nutrient N deficient Si deficient replete % dw % dw % dw Nutrient replete Td (h) g L−1 day−1 7 72 Nutrient replete g m−2 day−1 Nutrient replete 7 27 36 31 21 26 0. 26 Gatenby et al. 29 Greque de Morais et al. 43. 5 Becker (1994). 15.34 13 50 Literature Nutrient replete mg L−1 day−1 Referencesc Calculated Nutrient replete mg L−1 day−1 Species Taxaa Cy C H H B F F M M M 11. 47 Moheimani (2005). 71 Tomaselli et al. 52. 27. 45 McGinnis et al. 42. 54 Patil et al. 23 Exley et al. (2008). 31 Haury and Spiller (1981). 2 Ahmad and Hellebust (1990). 7 Benider et al. 43. 35 Janssen et al. 38.51 35 17 25 35 13 Oscillatoria Ourococcus Pavlova lutheri Pavlova salina Phaeodactylum tricornutum Porphyridium purpureum Prymnesium parvum Scenedesmus dimorphus Scenedesmus obliquus Scenedesmus quadricauda Selenastrum gracile Skeletonema costatum Spirulina maxima Spirulina platensis Synechococcus Tetraselmis suecica Thalassiosira pseudonana Thalassiosira weissflogii Tribonema M M F F F F M S S M M M M M 16 32 14 9 36 12 14 44 19 23 22 5. 55. (1987). (2007). 74 Xu et al. (2007). Cy Cyanobacteria. 41 Lu et al. (1996). 43 Mansour et al. 12. (1997). 42. 15 Chisti (2007).08 0. 37. 63 10.19 0. E Eustigmatophyta. 65 Shifrin and Chisholm (1981). (1998). (1969). 60 Richardson et al. 28 Goldman and Peavey (1979). 44 Matsukawa et al. 52 Ostgaard and Jensen( 1982). 61. 55. 38. D Dinophyta. (2000). (2007). 47. 16 Coleman et al. 25 Fisher et al. 17. 61 61 13. 59 5. 72 Ugwu et al. (1987). 67 61 65 24. 71. 17 Collyer and Fogg (1954). 30. 50 Mourente et al. (1989). (2000). 49 Moore (1975). 46 McKnight (1981). (1976). (1994). 48 Moheimani and Borowitzka( 2006). S saline c Key to references: 1 Adam (1997). (1967). 40 Liu et al. 6 Ben-Amotz and Tornabene (1985). 54 11 30 26 21 18 21 16 7 13 11 17 16 22 12 0. 37 Lee and Bazin (1991). 55 5. (1996). 17. 26. M marine. 65. 20 Coombs et al. 12 Butterwick et al. (2002). (1987). Eg Euglenozoa. (2000). (1994). 38 Lee (2001). (2005). (2008). H Haptophyta. (1993). 17. 73 5. 32 Hu and Gao (2003). 11 Burlew (1953). 49. 8 Beudeker and Tabita (1983).59 0. 61 Rodolfi et al. 58 Reitan et al. 4 Baker et al. 5 5. (2005). 39 Li et al.16 0.23 R H C C C C O Cy Cy Cy P O O O 75 32 17 99 13 59 50 52 Average Blank indicates no information available a Key to taxa: C Chlorophyta. 38. 21 De la Pena (2007).

The diatoms and other taxa have a wider distribution under Nsufficient conditions. Fig. dashed lines nitrogen deprived) 100 90 Lipid content (% dw) 80 70 60 50 40 30 20 10 Scenedesmus quadricauda Scenedesmus acuminatus Chlamydomonas applanata Ankistrodesmus falcatus Anabaena cylindrica Chlamydomonas reinhardtii Chlorella pyrenoidosa Chlorella sorokiniana Ettlia oleoabundans Spirulina maxima Chlorella vulgaris Spirulina platensis Thalassiosira pseudonana Scenedesmus obliquus Chlorella minutissima Chlorella emersonii Chlorella protothecoides Monoraphidium minutum Scenedesmus dimorphus Nitrogen replete 499 Nitrogen deprived Cyanobacteria The average laboratory lipid content for other taxa (including diatoms. Ochrophyta. The response to nitrogen deprivation was varied. golden algae. Dinophyta. nitrogen-deprived and silicondeprived conditions for Dinophyta. On silicon deprivation. with one species dropping below 10% and an increase in the number of species between 40% and 50% Nitrogen replete Nitrogen deficient Silicon deficient Hymenomonas carterae Isochrysis galbana Navicula acceptata Skeletonema costatum Chaetoceros calcitrans Amphiprora hyalina Monodopsis subterranea Phaeodactylum tricornutum Chaetoceros muelleri Nannochloropsis salina Prymnesium parvum Dunaliella tertiolecta Tetraselmis suecica Euglena gracilis Navicula saprophila Pavlova lutheri Pavlova salina Amphora Thalassiosira weissflogii Dunaliella primolecta Dunaliella salina Nitzschia dissipata Nannochloropsis Cylindrotheca Nitzschia frustulum Cyclotella cryptica Porphyridium purpureum Navicula pelliculosa Crypthecodinium cohnii Nitzschia communis Nitzschia palea Tribonema Synechococcus Nannochloris Ourococcus Oscillatoria 0 . 3b). with seven showing a decrease or no change. 1 Average laboratory lipid content under nutrient-replete (open circles) and nitrogen-deprived (filled circles) conditions for Chlorophyta and Cyanobacteria. 2. 2 Average laboratory lipid content under nutrient-replete. The varied response to nutrient deficiency is demonstrated by the resultant bimodal distribution. Nitrogen-replete lipid content ranges from 11% to 51% dw. 3. Haptophyta. with an average of 25%. Euglenozoa. Most of the Chlorophyta have a lipid content between 20% and 30% dw under N-sufficient conditions. Under N deprivation. showing the shift in lipid contents with N deficiency for Chlorophyta (Fig. a shift in lipid content to the right is clearly seen with resultant contents from 18% to 64%. the average lipid content increased from 24% to 41% dw. dashed lines nitrogen deprived) 100 90 80 Lipid content (% dw) 70 60 50 40 30 20 10 0 The effect of nutrient depletion is further demonstrated in Fig. Error bars show the minimum and maximum recorded values for each species (solid lines nitrogen replete and silicon deprived. Ochrophyta and Prasinophyta. Error bars show the minimum and maximum recorded values for each species (solid lines nitrogen replete. nitrogen-deprived and silicon-deprived conditions are summarised in Fig. 3a) and other taxa (Fig. Haptophyta. Prasinophyta and Eustimatophyta) under nutrientreplete. similar to that for green algae. Euglenoza. Seventeen of 24 species for which information was available showed an increase in lipid content. The average lipid content with nitrogen deprivation was 27%. Eustigmatophyta.J Appl Phycol (2009) 21:493–507 Fig.

88 day−1). The next most productive strains are the marine Tetraselmis suecica (99 mg L−1 day−1) and the freshwater C. along with those for the Cyanobacteria Synechococcus. and 164 calc. The greater nitrogen-deprived lipid content for freshwater species is largely because most green algae (which show a greater response to nitrogen deprivation) are freshwater species. Biomass productivity Typical algal growth rates are reported in Figs. Average nutrient-replete and nitrogen-deficient lipid content. Lipid productivity was calculated as the product of average nutrient-replete lipid content and biomass productivity in grams per litre per day. Prasinophyta dw lipid. The lipid productivities of E. (1998). The lipid productivity for Amphora is the average of values for three different strains.96 day−1). collected by M. This may account for the wide spread of recorded lipid productivities (63 to 345 mg L−1 day−1. both with very high growth rates (0.38 day−1). 3 Number of algal species in each lipid content category under nutrient-sufficient. oleoabundans and A. The overall average lipid productivity for all species from literature was 50 mg L−1 day−1 compared with a calculated value of 52 mg L−1 day−1. were measured by Nile Red staining as triolein equivalents (Sheehan et al. A high doubling time corresponds to a low specific growth rate. This limits the accuracy of these measurements. 1998). where available.08–2. Euglenozoa. Haptophyta. rather surprisingly given its low lipid content. 6). above 100 mg L−1 day−1: Amphora (160 mg L−1 day−1 lit. a major problem with Nile Red is that species vary widely in their ability to take up this lipophilic dye. known as AMPHO27. respectively. 4 and 5 as the average doubling time for each species. Species grown under Si deficiency have lipid content between 30% and 50% dw.69 day−1. falcatus are a function of their high growth rates (0. nitrogen and silicon-deficient conditions. 6 and supplemented with calculated (calc. There has been no rigorous comparison of Nile Red staining and lipid quantitation across species. According to Sheehan et al. The average doubling time calculated for Average lipid productivities collected from literature (lit.59 and 0. and for other taxa 18 h (μ= 0.55 g L−1 day−1.). has a relatively high lipid productivity (75 mg L−1 day−1). Sommerfield. sorokiniana (97 mg L−1 day−1). as shown by the error bars in Fig.) are summarised in Fig. AMPHO45 and AMPHO46. mg L−1 day−1) and Ankistrodesmus falcatus (109 mg L−1 day−1 calc. 6. respectively are 22% and 36% for freshwater species and 24% and 28% for marine and saline species.). respectively) and below average lipid content (17% and . When species are grouped according to culture environment rather than taxa. b Dinophyta. three species stand out as having very high lipid productivities. Lipid productivity 2 0 0-10 10-20 20-30 30-40 40-50 50-60 60-70 Lipid content (% dw) 14 12 Number of species (b) N replete N deficient Si deficient 10 8 6 4 2 0 0-10 10-20 20-30 30-40 40-50 50-60 60-70 Lipid content (% dw) Fig. corresponding to a μ of 0.500 J Appl Phycol (2009) 21:493–507 14 12 Number of species (a) N replete 10 8 6 4 N deficient the top 20% of Chlorophyta. Ochrophyta. Average doubling time for freshwater species is 20 h (μ=0.92 day−1).46 g L−1 day−1) and lipid contents of 36% and 24% dw. 1986–1987 (Sheehan et al. no dominant trend in growth rates or lipid contents is seen. Cyanobacteria and other taxa with respect to growth rate all lie in the range 7 to 8 h (μ=2. Productivities under nutrient-deprived conditions were not included due to a lack of reported growth rates under these conditions. These values. a Chlorophyta. From Fig. which. The average doubling time for green algae is 24 h.83 day−1) while that for marine or saltwater species is 19 h (μ=0. Ettlia oleoabundans (formerly Neochloris oleoabundans) (136 lit. The high lipid productivity of Amphora is the product of a high reported lipid content (average 51% dw) and a modest growth rate (Td =20 h). 1998). The average doubling time for Cyanobacteria is 17 h (μ=0.) lipid productivity. No obvious trend in lipid productivity with taxonomy or culture environment (fresh versus marine) was noted.

36% and 26% dw. Productivity in outdoor photobioreactors was on average five times higher than in the laboratory. Further. Error bars represent highest and lowest recorded values 100 90 Doubling time (hours) 80 70 60 50 40 30 20 10 0 Chlamydomonas reinhardtii Scenedesmus acuminatus Chlorella protothecoides Chlorella sorokiniana Scenedesmus dimorphus Chlorella pyrenoidosa Chlorella vulgaris Monoraphidium minutum Chlorella emersonii Chlorella minutissima Anabaena cylindrica Spirulina maxima Ankistrodesmus falcatus Spirulina platensis 501 Cyanobacteria 18% dw). Overall biomass productivities in grams per square metre per day and grams per litre per day were 130% and 96%. Average lipid productivities reported for these range from 97 to 160 mg L−1 day−1. As rigorous data on nutrient deficiency and growth rate are not available across sufficient species. Contrary to the popular belief that the large metabolic demand of high lipid content necessitates slow growth rate. C. However. 28%.23. These four species are reported to have average to good growth rates (0. Lipid content in outdoor ponds was very similar to that under laboratory conditions. the top three biomass producers are not the top lipid producers. Pavlova lutheri (75 mg L−1 day−1) and Phaeodactylum tricornutum (72 mg L−1 day−1). respectively) and average or above lipid content (31%. summarised in Fig. indicating that lipid content is also a factor. The species with a high lipid productivity (>60 mg L−1 day−1) range in lipid content from 11% dw to 51%. A general correlation is demonstrated between lipid productivity and biomass productivity. 7. greater than 60 mg L−1 day−1. suecica. These are followed by Nannochloropsis (82 mg L−1 day−1).4 g L−1 day−1) and most those above 0.27. Lipid content does not correlate directly with lipid productivity. 4 Average doubling time for Chlorophyta and Cyanobacteria. Discussion Most promising species in terms of lipid productivity Analysis of lipid content. The two species with the highest lipid contents (51% and 33% dw) maintain average to good doubling times of 20 and 10 h. The overall average lipid content for the 20 species in outdoor ponds was 110% of that in the laboratory.J Appl Phycol (2009) 21:493–507 Fig. there appears to be no significant correlation between these. These data. A. Information was found for only 19 of the 55 species reported in Table 3.21 and 0. All species with a high biomass productivity (above 0. Figure 8 shows lipid content as a function of doubling time. oleoabundans. of light) are not comparable. sorokiniana and T. Nannochloris (77 mg L−1 day−1). E. respectively. In Fig.g. This is contrary to the expectation that productivities achieved in outdoor ponds are generally lower than those in the laboratory. highlight the following species for high lipid productivity: Amphora. falcatus. While these species Synechococcus Nannochloris Ourococcus Oscillatoria . species with a high lipid content (>40%) vary in lipid productivity between 17 and 160 mg L−1 day−1. Comparison of laboratory data with outdoor pond and photobioreactor data Table 4 shows the average literature data for microalgal species grown outdoors in open ponds or closed photobioreactors. respectively). This may be due to the limited available dataset or because conditions (e. this is not included in the review. respectively of that under laboratory conditions. 0. a clear relationship is needed. 6. In order to exploit nutrient limitation to maximise lipid content and productivity. further indicating that lipid content alone is not a good indicator of suitability for biodiesel production.2 g L−1 day−1 have a high lipid productivity. the impact of biomass productivity and lipid content on lipid productivity under nutrient-replete conditions is analysed through correlation. The ratio of productivity outdoors to productivity in the laboratory is compared. 0. biomass productivity and their combination to yield lipid productivity has been conducted across literature data collected on 55 algal species under nutrient-replete conditions.34 g L−1 day−1.

the incompleteness of the dataset (lipid productivity only available or discernable for 25 of the 55 species studied on a volumetric basis to allow direct comparison) and the varying extent of optimisation imply that other species may be added to this grouping as data become available. hence. comparison of lipid productivities across algal species has been restricted to laboratory lipid content under nutrient-sufficient conditions.502 100 90 80 J Appl Phycol (2009) 21:493–507 Doubling time (hours) 70 60 50 40 30 20 10 0 Porphyridium purpureum Dunaliella tertiolecta Phaeodactylum tricornutum Skeletonema costatum Navicula saprophila Euglena gracilis Nannochloropsis Prymnesium parvum Dunaliella salina Navicula acceptata Navicula pelliculosa Nitzschia dissipata Cylindrotheca Thalassiosira pseudonana Chaetoceros muelleri Crypthecodinium cohnii Nitzschia communis Isochrysis galbana Hymenomonas carterae Tetraselmis suecica Amphiprora hyalina Cyclotella cryptica Thalassiosira weissflogii Tribonema Amphora Fig. 6 Average literature (dark grey bars) and calculated (light grey) values for biomass productivity (milligrams per litre per day). Lipid content reported under N. The response to nutrient deficiency has been shown to vary across species. it is dependent on both. nitrogen stress correlates well with increased lipid content (Fig. but lipid content has not been shown to be a reliable indicator of lipid productivity. 5 Average doubling time for other taxa. Fig. Error bars show the minimum and maximum recorded lipid productivity for literature values and propagation of error for calculated values 350 In this study. It is clearly illustrated that lipid content may be enhanced by nutrient stress. A positive increase Lipid productivity (mg. 3a).L . respectively. In Chlorophyta.and Si-deficient conditions were on average 138% and 168% of nutrient-sufficient lipid contents reported.day ) -1 -1 300 250 200 150 100 50 0 Ankistrodesmus falcatus Synechococcus Nitzschia palea Scenedesmus quadricauda Porphyridium purpureum Ettlia oleoabundans Tetraselmis suecica Nannochloropsis Scenedesmus obliquus Thalassiosira pseudonana Nannochloris Phaeodactylum tricornutum Chaetoceros calcitrans Monodopsis subterranea Skeletonema costatum Chlorella minutissima Chlorella sorokiniana Isochrysis galbana Tribonema Amphora Pavlova lutheri Pavlova salina Chlorella vulgaris Chaetoceros muelleri Chlorella emersonii . 3b). Lipid productivity is the product of lipid content and biomass productivity. whereas a more dominant correlation was observed between biomass and lipid productivity. Error bars represent highest and lowest recorded values have exhibited promise with respect to lipid productivity. whereas the response of other taxa to nitrogen stress is more varied (Fig.

4 -1 0 .) with biomass productivity (a) and lipid content (b) under nutrient-replete conditions in lipid content with silicon deficiency is reported across the diatoms.6 -1 0 .L . 7 Correlation of lipid productivity (average of lit.1.day -1) 140 120 100 80 60 40 20 0 0 . If they require culture on solid substrates. underutilised as illustrated by only being reported for 20 of the 55 species presented here. From a practical perspective. 2008). living in the lowest level of a body of water. two-stage culture with initial optimisation of biomass and final optimisation of lipid content Lipid content (% dw) Fig. this may render them unsuitable for large-scale production due to harvesting complexity. 2008). Using the indicator of lipid productivity across the duration of the production phase is seen to be particularly important under conditions of 80 70 Doubling time (hours) 60 50 40 30 20 10 0 0 20 40 60 Lipid content (% dw) Fig. 8 Doubling time versus lipid content under nutrient-replete conditions . Furthermore.g.0 benefits volumetric lipid yield. improve the efficiency of biomass processing (Rodolfi et al. there are cases where nitrogen deprivation has been shown to improve lipid productivity in the short term. e.L -1 . Cylindrotheca and Nitzschia are all benthic diatoms (Chen 2007). insufficiently rigorous data on the impact of nutrient limitation on biomass productivity limit comparison of lipid productivity under nutrient deficiency on a species basis. The response of biomass productivity to nutrient limitation has been shown to vary widely between species (Rodolfi et al. However. however. Lipid productivity can be calculated as the product of biomass productivity (grams dry weight per litre per day) and lipid content (% dw) to give an indicator of oil produced on a basis of both volume and time.day ) 180 (b) 160 Lipid productivity (mg.L . Nannochloropsis (Rodolfi et al. Certain species may be able to be grown planktonically with sufficient agitation. It is.8 Biomass productivity (g. Navicula. The translation of an increase in lipid content into an increase in lipid productivity is dependent on the degree of growth retardation caused by the nutrient deficiency. as faster growing species may demonstrate lipid productivity greater than those with a very high lipid content. Currently. Lipid content reported in the absence of growth rate or biomass productivity does not allow rational species selection for lipid production. 2008). and calc.J Appl Phycol (2009) 21:493–507 503 180 (a) 160 Lipid productivity (mg.day -1 ) 140 120 0 80 60 40 20 0 0 20 40 60 Lipid productivity is a critical variable for evaluating algal species for biodiesel production. A high lipid content may. Enhanced lipid content and growth retardation under nutrient deficiency often counterbalance one another. it should be noted that Amphora.2 0 . however. The importance of reporting lipid productivity 0 . often attached to the substrate bottom.

98 Biomass productivity g m−2 day−1 Biomass productivity g L−1 day−1 Biomass productivity g L−1 day−1 Lipid content Ratio Biomass productivity Ratio Biomass productivity Ratio Calculated ratio of averages Biomass productivity Ratio References Outdoor ponds Outdoor PBR Outdoor pond/laboratory PBR/laboratory Species Taxa 26 3. 47 38.30 28 0.28 21 16 0. 63 63 13.96 0.18 1. 55 63 47 38.60 Amphora Anabaena cylindrica Ankistrodesmus falcatus Chaetoceros muelleri Chlorella pyrenoidosa Chlorella vulgaris Cyclotella cryptica Dunaliella salina Isochrysis galbana Monodopsis subterranea Monoraphidium minutum Nannochloropsis Nannochloropsis salina Phaeodactylum tricornutum Porphyridium purpureum Scenedesmus obliquus Spirulina maxima Spirulina platensis Tetraselmis suecica 22 26 24 11 19 0.44 0.49 0. 63 41.95 0.05 0.30 B Cy C O C C O Pr H E C E E B R C Cy Cy P M F F M F F M S M F F M M M M F S S M 63 46 63 63 38.07 0.33 1.68 1.69 0.38 2.10 0.96 5.02 1. Ratios have been generated by dividing outdoor values by corresponding laboratory values in Table 3.504 Table 4 Average lipid content and biomass productivity from literature for microalgae grown in outdoor ponds and photobioreactors under nutrient-replete conditions Media Average from literature Lipid content % dw 40 39 0.13 5. 38.44 0. 47.35 1.17 1. 57 63 47.25 1.85 0.58 0. 63 30 38 38.15 Blank indicates no information available.33 1.29 0.80 0. 55 63 Average 0.18 7.79 0.10 1.36 15 25 1.99 1.78 5.18 0.27 1.20 0.50 6.18 48 0.39 0. 63 11. 61.53 1. media and references as in Table 3 PBR photobioreactors J Appl Phycol (2009) 21:493–507 . Keys to taxa.90 24 35 22 26 14 16 27 2.76 0.

pH. determining the resilience of species by measuring the range of environmental conditions (e. Hence. absolute comparison cannot be made. using a variety of strains. To refine selection.e. light. Biomass concentration. emanating from the level of development of the current algal literature. most typically on a basis of volume or area. the culture conditions of selected promising species could be optimised individually to provide a measure of the maximum biological productivity expected. as well as ease of harvesting and downstream processing. In addition to the key indicator of lipid productivity. The body of literature on algal culture and algal lipid content has been collected for a variety of purposes. culture vessels and locations. temperature. Lipid contents and biomass and lipid productivities. including the production of food.) within which the algae remains productive and determining ease of algal cell harvesting (e. resources available. particularly with respect to characterising optimum growth conditions. but the data can be used to identify key species with potential for further experimental work. species must be tested either under their optimal conditions. This would select for species ideal for that particular location and system. light. feed. characteristics such as ease of cultivation and harvesting are vital to the success of any large-scale algae culture facility and a sufficient data inventory of these factors remains to be generated.g. A set of standard conditions as close to those expected in the large-scale culture facility as possible could be used to screen species in the laboratory. However. pH. 2000). To ensure maximum value of the data presented. this review provides a starting point for further investigation. Reactor geometry is required for their inter-conversion. A single species can have a variety of strains with widely different characteristics. demanding further experimental study. Resistance to contamination. by flocculation. the former being the product of biomass productivity and lipid content while the latter is the product of specific growth rate and biomass concentration. fuel and fine chemicals.g. tolerance of operating conditions such as light. hence. In conclusion. is frequently not reported. toxicity and environmental studies. with different equipment and protocols. CO2 levels. insufficient published information currently exists to enable comparison across these aspects of a variety of species. location and prevailing environmental conditions. it is necessary that growth rates be reported in standard units. nitrogen deprivation). filtration or sedimentation). or the expected operational conditions at large scale. algal growth may be presented as a productivity or growth rate. temperature. Similarly. Acknowledgements This work is based upon research supported by the South African Research Chair Initiative of the Department of Science and Technology and the National Research Foundation. The road ahead Owing to the limitations discussed above. while frequently decreasing growth rate (Illman et al. volumetric lipid and biomass productivity are recommended. although key characteristics for biodiesel production.g. However. ionic strength and flue gas toxins. also impact the success of large-scale culture. etc. Many studies do not present optimised data. The species is not always identified correctly in studies. this paper demonstrates the role of information available in the literature in providing earlystage guidance on species selection. as well as the scope and aims of the individual project in question. The final choice of algal species is governed by the culture system used. While such review is essential to inform species selection. References Adam MS (1997) Metabolic response of the halotolerant green alga Dunaliella bardawil to nitrogen:phosphorous ratios in batch culture. Experiments have been conducted under different conditions. as well as taxonomic. measuring growth rates under conditions that enhance lipid content (e. The financial assistance of the National Research Foundation (NRF) towards this research is hereby acknowledged. Lipid productivity is presented on a range of bases. nutrient requirements. with classification often restricted to a genus level. constraints are recognised. Limitations This review summarises information available in open source literature on the lipid productivity of microalgae. Folia Microbiol 42:357–360 . fluctuating temperatures and light intensities). Alternatively. Here. The culture system would then be designed to mimic these conditions. Sufficient information should be provided for their inter-conversion. key for their inter-conversion. with the aim of facilitating the choice of algal species for large-scale biodiesel production. are not the only characteristics to be considered to ensure a cost-effective and feasible biodiesel production process. media composition. temperature. A further constraint is that algal taxonomic definition has lagged behind other systems. these data remain incomplete. complete reporting of culture conditions on reporting productivities is key to maximising data available for comparison. nutrient levels.J Appl Phycol (2009) 21:493–507 505 nutrient deprivation known to enhance lipid content in several algae species. Opinions expressed and conclusions arrived at are those of the authors and are not necessarily to be attributed to the NRF. nutrient levels. measuring lipid productivity under outdoor conditions (i.

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