Bioresource Technology xxx (2007) xxx–xxx


Photobioreactors for mass cultivation of algae
C.U. Ugwu *, H. Aoyagi, H. Uchiyama
Institute of Life Sciences and Bioengineering, University of Tsukuba, 1-1-1 Tennodai, Tsukuba City, Ibaraki 305-8572, Japan Received 16 October 2006; received in revised form 30 January 2007; accepted 31 January 2007

Abstract Algae have attracted much interest for production of foods, bioactive compounds and also for their usefulness in cleaning the environment. In order to grow and tap the potentials of algae, efficient photobioreactors are required. Although a good number of photobioreactors have been proposed, only a few of them can be practically used for mass production of algae. One of the major factors that limits their practical application in algal mass cultures is mass transfer. Thus, a thorough understanding of mass transfer rates in photobioreactors is necessary for efficient operation of mass algal cultures. In this review article, various photobioreactors that are very promising for mass production of algae are discussed. Ó 2007 Elsevier Ltd. All rights reserved.
Keywords: Algae; Biomass; Mass transfer; Mixing; Photobioreactors

1. Introduction Algae are grown either in open culture systems or closed systems (photobioreactors). Early attempts to grow algae in open ponds were conceived by Germans (Europe) during the world war II. At that time, algae were grown mainly as food supplements. As industrialization began, some groups of workers in Carnegie Institute at Washington implemented mass cultivation of algae for CO2 abatement (Burlew, 1953). Between early 1970s and late 1970s, commercial production of algae was initiated in East Europe, Israel and Japan. During these periods, algae were grown commercially in open ponds as healthy food. In Africa, Lake Chad and Lake Texcoco were the major sources of Spirulina biomass for the people living in those areas. As a matter of fact, the purpose of growing algae depended on the specific needs of the people. In the United States, algal pond systems were developed for water treatment. The biomass recovered was converted to methane, which was a major source of energy (Burlew, 1953; Oswald and Golueke,


Corresponding author. Tel./fax: +81 29 853 7212. E-mail address: (C.U. Ugwu).

1960). As time went on, algal biomass became very important in the field of aquaculture (Muller-Feuga, 2000). Recently, algae have attracted much attention due to their potentials in the production of fine chemicals (Borowitzka, 1999; Lorenz and Cysewski, 2000) and as useful supplements in humans and animals (Dallaire et al., 2007). Algae have also found application in other areas such as in immobilization systems for production of some extracellular compounds (Chetsumon et al., 1994), and also for biosorption of heavy metals (Wilde and Benemann, 1993; Lodeiro et al., 2005; Karthikeyan et al., 2007). Some studies have also indicated the importance of algae in carbon dioxide fixation (Benemann, 1997; Sung et al., 1999; Chae et al., 2006). Given the advantages of closed systems over open ponds, a good number of them (ranging from laboratory to industrial scale) photobioreactors have been proposed. Closed photobioreactors have attracted much interest because they allow a better control of the cultivation conditions than open systems. With closed photobioreactors, higher biomass productivities are obtained and contamination can be easily prevented. It is anticipated that algal biotechnology would pave way to the development of Closed Ecological Life Support System (CELSS) (Lee and Palsson, 1995; Cogne et al., 2005). Despite that a good number of

0960-8524/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.biortech.2007.01.046

Please cite this article in press as: Ugwu, C.U. et al., Photobioreactors for mass cultivation of algae, Bioresour. Technol. (2007), doi:10.1016/j.biortech.2007.01.046

easy to sterilize. high potentials for scalability.1016/j. torus (Pruvost et al.. 1999). some degree of wall growth. One of the major setbacks in mass production of algae is lack of efficient photobioreactors. low energy consumption. cultures are easily contaminated Small illumination surface area. lagoons. / Bioresource Technology xxx (2007) xxx–xxx photobioreactors have been investigated. Also. Naturally illuminated algal culture systems with large illumination surface areas include open ponds (Hase et al. Also. C. relatively cheap. their construction require sophisticated materials. Tempering could simply be achieved by placing a photobioreactor in a constant temperature room. 2. suitable for outdoor cultures. From this point of view. easy to clean up after cultivation. readily tempered. some photobioreactor designs that are promising for mass cultivation of algae are critically examined. et al. 1997). such as double-walled internally-illuminated photobioreactor with a heating and cooling water circuit (Pohl et al. 2003). due to inefficient stirring mechanisms in open cultivation systems. limited to few strains of algae. major limitations in open ponds include poor light utilization by the cells. and stirred-tank have good scalability though their use in outdoor cultures is limited since they have low illumination surface areas. 1996.. laboratory-scale photobioreactors are artificially illuminated (either internally or externally) using fluorescent lamps or other light distributors. good biomass productivities. Technol. 2. good for mass cultivation of algae Limitations Little control of culture conditions. difficulty in controlling culture temperature. requires large land space Vertical-column photobioreactors Flat-plate photobioreactors Tubular photobioreactors High mass transfer.2007. ponds) and artificial ponds or containers. circular ponds and raceway ponds... However.) can be readily tempered. Photobioreactors such as bubble-column. flat-plate (Hu et al. doi:10. reduced photoinhibition and photo-oxidation Large illumination surface area. poor productivity. 1998) photobioreactors. Largescale outdoor systems such as tubular photobioreactors cannot be easily tempered without high technical efforts... 2006).. Bioresour. some efforts were undertaken to design temperature-controlled photobioreactors. some degree of wall growth. easy to clean up. airlift column (Harker et al. Tredici and Materassi.. 2000). horizontal/serpentine tubular airlift (Camacho Rubio et al. for example. readily tempered.U. some aspects of hydrodynamics and mass transfer characteristics of these photobioreactors are briefly discussed. This approach is limited to compact photobioreactors. and seaweedtype (Chetsumon et al. Ugwu et al. Kaewpintong et al. 1988. several commercially available photobioreactors. tanks. Generally. 1999). Furthermore. 1988).biortech. Photobioreactors Algal culture systems can be illuminated by artificial light. One of the major advantages of open ponds is that they are easier to construct and operate than most closed systems. 2001... good for immobilization of algae. good mixing with low shear stress. 1996). relatively cheap Please cite this article in press as: Ugwu. their mass transfer rates are very poor resulting to low biomass productivity. evaporative losses. (2007)... Some of these photobioreactors include bubble column (Degen et al. contamination by predators and other fast growing heterotrophs have restricted the commercial production of algae in open culture systems to only those organisms that can grow under extreme conditions. 2002. BIOSTAT photobioreactors (developed by Sartorius BBI Systems Inc. helical tubular (Hall et al. Photobioreactors for mass cultivation of algae. Chini Zittelli et al. 1992. 2007). horizontal and inclined tubular photobioreactors are promising except for the difficulty in scaling them up. conical (Watanabe Table 1 Prospects and limitations of various culture systems for algae Culture systems Open ponds Prospects Relatively economical. possibility of hydrodynamic stress to some algal strains Gradients of pH. Open ponds Cultivation of algae in open ponds has been extensively studied in the past few years (Boussiba et al.. However. a thorough understanding of some aspects of hydrodynamic and mass transfer of photobioreactors is required. shear stress to algal cultures. To improve algal productivity. suitable for outdoor cultures.U. Ogbonna et al. stirred-tank (Ogbonna et al. Open ponds can be categorized into natural waters (lakes. In this review article. difficulty in growing algal cultures for long periods. good for immobilization of algae. and inclined tubular photobioreactors (Ugwu et al. airlift. Furthermore. Table 1 summarizes the advantages and limitations of open ponds. occupy large land mass.046 .1. solar light or by both. dissolved oxygen and CO2 along the tubes. 2000).. diffusion of CO2 to the atmosphere. and requirement of large areas of land. decrease of illumination surface area upon scale-up Scale-up require many compartments and support materials. low oxygen buildup Large illumination surface area. only very few of them can effectively utilize solar energy for mass production of algae.. some photobioreactors can be easily tempered. fouling.. fairly good biomass productivities. 2002). flat-plate.01. good light path. and Saiki. The most commonly used systems include shallow big ponds. Furthermore.ARTICLE IN PRESS 2 C. Hase et al.. Most outdoor photobioreactors are characterized by largely exposed illumination surfaces. 2003).

Technol. some studies have shown that very high dissolved oxygen (DO) levels are easily reached in tubular photobioreactors (Torzillo et al... 1999.. Air and CO2 are supplied to the cultures through the spargers.046 .5. The work presented by Milner (1953) paved way to the use of flat culture vessels for cultivation of algae. 2004). efficient light distribution to the cells can be achieved by improving the mixing system in the tubes (Ugwu et al. the cells at the lower part of the tube will not receive enough light for cell growth (due to light shading effect) unless there is a good mixing system. 1998)... Photobioreactors for mass cultivation of algae. Molina et al.. they also have some limitations as indicated in Table 1. 2006.01.. it is difficult to control culture temperatures in most tubular photobioreactors. For instance. conical (Watanabe and Saiki. Flat-plate photobioreactors Flat-plate photobioreactors have received much attention for cultivation of photosynthetic microorganisms due to their large illumination surface area. inclined (Lee and Low. It should also be noted that adherence of the cells of the walls of the tubes is common in tubular photobioreactors. 2002. Vertical-column photobioreactors are compact... As time went on.4.. tubular photobioreactor is one of the most suitable types for outdoor mass cultures. Tubular photobioreactor are very suitable for outdoor mass cultures of algae since they have large illumination surface area. (2007). intermixing occurs between the riser and the downcomer zones of the photobioreactor through the walls of the draft tube. Tubular photobioreactors Among the proposed photobioreactors. Ugwu et al. Ramos de Ortega and Roux (1986) developed an outdoor flat panel reactor by using thick transparent PVC materials. low-cost. and easy to oper´ nchez Miro ´ n et al. Although they can be equipped with thermostat to maintain the desired culture temperature. It has been reported that with flat-plate photobioreactors. 2000). In any case.2. Richmond et al. Bioresour. When a tubular photobioreactor is scaled up by increasing the diameter of tubes. The photobioreactor is equipped with impellers for agitation of the algal cultures. On the other hand. Following this work.. 1996. 1997). one of the major limitations of tubular photobioreactor is poor mass transfer. Vega-Estrada et al. Garcı et al. A summary of the prospects and limitations of vertical-column photobioreactors is shown in Table 1. 2. 2003). high photosynthetic efficiencies can be achieved (Hu et al. Vertical-column photobioreactors Various designs and scales of vertical-column photobioreactors have been tested for cultivation of algae (Choi ´ pez ´a-Malea Lo et al.biortech. et al. Most outdoor tubular photobioreactors are usually constructed with either glass or plastic tube and their cultures are re-circulated either with pump or preferably with airlift system. Hu et al. 2005a). 2002) photobioreactor.U. vertical (Pirt et al. Molina et al. this could be very expensive and difficult to implement.3. much attention is now focused on development of suitable closed systems such as flat-plate. Samson and Leduy (1985) developed a flat reactor equipped with fluorescence lamps. It should be noted that mass transfer (oxygen build-up) becomes a problem when tubular photobioreactors are scaled up.. 2002).2007. which would consequently increase the cost of algal production.. 2003. tubular. In the case of draft tube photobioreactors.. Ugwu et al.. the length of the tube can be kept as short as possible while a tubular photobioreactor is scaled up by increasing the diameter of the tubes. 1986. It was reported that bubble-column and airlift photobioreactors (up to 0.19 m in diameter) can attain a final biomass concentration and specific growth rate that are comparable to values typically reported for narrow ´ nchez Miro ´ n et al. Richmond. 2007). the illumination surface to volume ratio would decrease. extensive works on various designs of vertical alveolar panels and flat plate reactors for mass cultivation of different algae were reported (Tredici and Materassi. C. tubular photobioreactors (Sa Some bubble column photobioreactors are equipped with either draft tubes or constructed as split cylinders.1016/j. 1992. 2003. Fig. 2.. vertical-column and internally-illuminated photobioreactors.. / Bioresource Technology xxx (2007) xxx–xxx 3 In order to overcome the problems with open ponds.. Generally. 1983). The increase in pH of the cultures would also lead to frequent re-carbonation of the cultures. Zhang et al.. 1 shows a typical internally-illuminated photobioreactor. In this case. 1988. some photobioreactors can be internally illuminated with fluorescent lamps.. 1996. 2002). photoinhibition is very common in outdoor tubular photobioreactors (Vonshak and Torzillo. flatplate photobioreactors are made of transparent materials for maximum utilization of solar light energy. Ugwu et al. Kaewpintong et al. Furthermore. Also.U. doi:10.. A year later. Furtherate monoseptically (Sa more. 2001). Internally-illuminated photobioreactors As mentioned earlier. Advantages and limitations of tubular photobioreactors are shown in Table 1. long tubular photobioreactors are characterized by gradients of oxygen and CO2 transfer along the tubes (Camacho Rubio et al. 1993. However. Hoekema et al. Flatplate photobioreactors are very suitable for mass cultures of algae. This type of photobioreactor can also Please cite this article in press as: Ugwu. Aeration and mixing of the cultures in tubular photobioreactors are usually done by air-pump or airlift systems. near horizontal (Tredici and Chini Zittelli. they are very promising for large-scale cultivation of algae. 2001). Accumulation of dissolved oxygen concentrations in flat-plate photobioreactors is relatively low compared to horizontal tubular photobioreactors. 1991. They can be in form of horizontal/serpentine (Chaumont et al. 2. On the other hand. Also.ARTICLE IN PRESS C. 2005. 2. 2002).

2000. would increase the gas bubble velocity. Photobioreactors for mass cultivation of algae. 2002). resulting to poor mass transfer rates. contamination can be minimized. demarcation exists between the light-illuminated and dark surfaces. 1999). gas bubble velocity and gas holdup. mixing. surfactants/antifoam agents and temperature. outdoor mass cultivation of algae in this type of photobioreactor would require some technical efforts. Various mixing systems are currently used in algal cultures depending on the type of photobioreactors. Increase in aeration rate would improve mixing. 2001).. Hydrodynamics and mass transfer characteristics of photobioreactors Although relationship between hydrodynamics and mass transfer has been extensively investigated and correlated in bioreactors for heterotrophic cultures.. 2005b. Tredici and Chini Zittelli. mixing time can also be measured by signal-response method using tracer and pH electrode (Camacho Rubio et al. When fine spargers are used to increase gas dispersion inside horizontal tubular photobioreactors. The overall mass transfer coefficient (kLa) is the most commonly used parameters for assessing the performance of photobioreactors. However... mixing can be done by bubbling air directly or indirectly via airlift systems (Ogbonna and Tanaka. computational fluid dynamics (CFD) was used to evaluate global mixing in torus photobioreactor (Pruvost et al. impellers were used in mixing algal cultures (Ogbonna et al. liquid circulation... gas and the walls of the tube.2007.. 2001. Gas bubble velocity is a measure of culture flow rates in tubular photobioreactors (plug flow regime) since algal cultures are circulated along with gas bubbles. 3. thereby..01. liquid velocity. 1998) or by installing static mixers inside the tubes (Ugwu et al. keep algal cells in suspension. However. supply of light to the photobioreactor can be maintained continuously (both day and night) by integrating artificial and solar light devices. 2006). Schematic diagram of an internally illuminated photobioreactor. the artificial light source is switched on whenever the solar light intensity decreases below a set value (during cloudy weather or at night). 1988. high aeration could cause shear stress to algal cells (Mazzuca Sobczuk et al. Degen et al. Hase et al. relatively large bubbles are produced. Furthermore.. et al.U. 1991). 2006. the bubble diameter increases. mixing aimed at inducing turbulent flow would result in high yield of algal biomass (Hu et al. Sato et al. only a few studies on these aspects are available in phototrophic cultures. Furthermore. The term kLa is generally used to describe the overall volumetric mass transfer coefficient in photobioreactors.. 2006). 1991). Good mixing would ensure high cell concentration. Mazzuca Sobczuk et al.. Bosca et al. Kaewpintong et al. 1999. 2000).. It was also reported that when the nutritional requirements are sufficient and the environmental conditions are optimized.. One of the major advantages of internally-illuminated photobioreactor is that it can be heat-sterilized under pressure and thus. Generally. the type of sparger. (1991) demonstrated that the productivity of alga is higher in mixed culture than in an unmixed one under the same condition. Thus mixing strategies should be introduced in cultures to circulate algal cells between the lightilluminated and dark regions of the photobioreactors (Molina Grima et al. paddle wheels were used to induce turbulent flow (Boussiba et al. Lee and Bazin (1990) defines mixing time as the time taken for a small volume of dye solution added to the liquid to transverse the reactor. Mixing systems that utilized baffles in bubble-column photobioreactors were also demonstrated in algal cultures (Merchuk et al. help nutrient distribution. doi:10. In that case. the overall mass transfer coefficient (kLa). In open pond systems.biortech. 2006).. / Bioresource Technology xxx (2007) xxx–xxx Rotor Aeration port Impeller Fluorescent lamp Reactor wall Internally-illuminated photobioreactor Fig. Mixing time can be defined as the time taken to achieve a homogenous mixture after injection of tracer solution.. Ugwu et al. 1985. In stirred-tank photobioreactors.1016/j. 1. Ugwu et al. Technol. 1999. In bubble-column and large diameter tubular photobioreactors.. and mass transfer between gas and liquid phases in algal cultures... improve gas exchange as well as reduce the degree of mutual shading and lower the probability of photoinhibition (Janvanmardian and Palsson. However. which consequently.. Mazzuca Sobczuk et al. mixing time is determined in photobioreactors using tracer substances such as dyes. (2007). The contact area between the liquid and the gas is reduced. Pruvost et al. Please cite this article in press as: Ugwu. However. Ugwu et al. Mixing time is a very important parameter in designing photobioreactors for various biological processes.ARTICLE IN PRESS 4 C. Hydrodynamics and mass transfer characteristics that are applicable in photobioreactors include. be modified in such a way that it can utilize both solar and artificial light system (Ogbonna et al. In tubular photobioreactors. 2007).. 2006. Gas bubble velocity and size of the bubbles are dependent on the liquid flow rate. The volumetric mass transfer coefficient (kLa) of photobioreactors is dependent on various factors such as agitation rate. The rate of gas circulation may be interrupted when baffles or static mixers are installed inside the reactors to increase gas dispersion. eliminate thermal stratification. Bioresour. 1996). 1999. 2006). By increasing the gas flow rate.U. There are also some reports on the use of optic fibers to collect and distribute solar light in cylindrical photobioreactors (Mori. C. 2003. Matsunaga et al.046 . the bubbles coalesce during flow to form interface between the liquid broth..

. the kLa of about 0. the kLa obtained was in range of 1. the mixer elements would help to break down the large bubbles into fine ones thereby. while many photobioreactors are easily operated at laboratory scale. the kLa reported in 2-L split-cylinder internal-loop airlift photobioreactors (which was used for cultivation of Haematococcus pluvialis cultures) was 0. It should be 0. Some degree of turbulence is required in photobioreactors to ensure that all the cells are frequently exposed to light (Carlozzi.002 sÀ1 at superficial gas velocity of 0.. liquid velocity is a measure of liquid flow and degree of turbulence in photobioreactors.02 m sÀ1) was obtained (Ugwu et al. 2003. 2002). In intense algal cultures.7 · 10À3 sÀ1.2007. Apparently..7 and 4. kLa of 0.002 0.1016/j.4–82 · 10À4) in 13-L bubble-column photobioreactor (which was tested for cultivation of Porphyridium sp.020 0. 2001).006 0. 1995. (2002) Vega-Estrada et al.024 m sÀ1. This can be estimated as the volume of the liquid displaced by the gas (expansion of liquid volume) due to aeration. Another important aspect of hydrodynamics which has been used in characterizing photobioreactor design is gas holdup. (1998) Ogbonna et al. cells can aggregate to form some clumps inside photobioreactors. C. (2004) reported that the nature (i.. 2003. the relationship between superficial gas velocity and the overall mass transfer coefficient (kLa) studied in various algal cultures can be evaluated (Table 2). it was reported that at superficial gas velocity of 0. which was tested for outdoor cultures of Phaeodactylum tricornutum. (2000) ´ n Ferna ´ ndez et al. 4. bubble velocity and the overall mass transfer coefficient in bioreactors (Lu et al.01. the kLa reported was about 0. These scale-up strategies are very challenging.009 0. doi:10.020 0. (1998) Camacho Rubio et al. Scale-up of photobioreactors can be done by increasing the length. At superficial gas velocity of 0.014 1. Some studies have indicated that relationship exists between superficial gas velocity. (2000) reported that by varying the superficial gas velocity (5. improving the mass transfer rates.e.006 sÀ1 was obtained at superficial gas velocity of ´ n Ferna ´ ndez et al. shape. Solid velocity is also a very important parameter for the determination of hydrodynamics and mass transfer characteristics of bioreactors. 1998).009 m sÀ1 (Zhang et al.. algal strains and cultures as well as the methods used for such studies.009 sÀ1(Vega-Estrada et al. Gas holdup is described as the fraction of the reactor volume taken by the gas. Furthermore.014 sÀ1 (Camacho Rubio et al. / Bioresource Technology xxx (2007) xxx–xxx 5 However. In the case of 200-L external-loop airlift tubular.. the kLa obtained was 0. Ugwu et al. Couvert et al.. By using 200-L airlift tubular horizontal photobioreactors (at superficial gas velocity of 0. In some photobioreactors.7–4. 2005).055 0.biortech.). Wongsuchoto et al.046 .... only few of them can be successfully scaled up to pilot scale. these clumps may settle such that they cannot be re-circulated uniformly along the tubes. (1999) Merchuk et al. (2002) Zhang et al. 2004).25 m sÀ1 (Acie noted that comparison of the kLa based on only superficial gas velocity could be misleading considering the differences in photobioreactor scales (volume). Pruvost et al. With 3-L flat plate photobioreactor (which was used for cultivation of Synechocystis aquatilis cultures).009 m sÀ1. Also. This kLa value was about the same as the one reported by Ogbonna et al. 2005). size. the kLa of about 0. et al..009 0. In concentric tube airlift photobioreactor (which was used for Phaeodactylum tricornutum cultures).024 kLa (sÀ1) 0. Acie (2001) Ugwu et al. as well as the overall mass transfer rate (kLa). Mass cultivation of algae A good number of photobioreactors can be used in production of various algal products..160 5. 2002).7 · 10À3 0. geometry. 1998. Technol. Bioresour. gas– liquid interfacial surface area and the overall mass transfer coefficient. Merchuk et al.003 sÀ1 (at superficial gas velocity of 0.16 m sÀ1).4–82 · 10À4 0. 1999). Vandu et al.020 0. kLa (Chisti.02 sÀ1 was obtained (Contreras et al. Gas holdup is very important in photobioreactor design as it determines the circulation rate. Some studies have demonstrated that relationship exist between gas holdup. solid velocity would give an indication of how algal cells can be uniformly transported along the tube length as the cultures are aerated. and porosity) and quantity of solids have an influence on the mass transfer of bioreactors.055 m sÀ1.250 0. (2007).U.ARTICLE IN PRESS C. Photobioreactors for mass cultivation of algae. height or the number of compartments of the culture systems (depending on the type of photobioreactor). 2006). In narrow bore tubes. Phaeodactylum tricornutum Chlorella sorokiniana Synechocystis aquatilis Haematococcus pluvialis References Contreras et al. In 6-L inclined tubular which was used for cultivation of Chlorella sorokiniana. (1998) (with 3-L internally-illuminated photobioreactor) for Chlorella pyrenoidosa cultures at superficial gas velocity of 0. bubble size. Couvert et al.U.. the gas residence time. mainly Table 2 Relationship between the superficial velocities and overall mass transfer coefficient (kLa) in various cultures systems Photobioreactor Concentric tube airlift Internally-illuminated Airlift tubular horizontal Bubble-column External-loop airlift tubular Inclined tubular Flat-plate Split-cylinder internal-loop airlift Volume (L) 12 3 200 13 200 6 3 2 Superficial velocity (m sÀ1) 0.003 0. diameter. (2005) Please cite this article in press as: Ugwu.009 Strain Phaeodactylum tricornutum Chlorella pyrenoidosa Porphyridium cruentum Porphyridium sp.

Given that outdoor photobioreactors are usually naturally illuminated using solar light. high mass transfer rates and should as well.U. 2006). Furthermore. Acie 2001).. it is difficult to carry out outdoor mass cultivation of algae all year round in such regions. J.27 Reference Camacho Rubio et al. intensive efforts should be made to increase the algal biomass productivity.06 0. Please cite this article in press as: Ugwu.05 0.U.. / Bioresource Technology xxx (2007) xxx–xxx Table 3 Productivity of algal strains reported in some outdoor photobioreactors Photobioreactors Airlift tubular Airlift tubular Airlift tubular Inclined tubular Undular row tubular Outdoor helical tubular Parallel tubular (AGM) Bubble-column Flat plate Volume (L) 200 200 200 6. about 0. CO2 mitigation with microalgal systems. 2001). In addition.. F. However. mixing. Furthermore. Ferna ´ ndez Sevilla. Photobioreactor development is perhaps. This is actually a very serious setback of algal cultivation in many developed countries. C. Photobioreactors for mass cultivation of algae. In 55L bubble column photobioreactor (for outdoor cultivation of Haematococcus pluvialis). 2001). high illumination surfaces. (2002) Carlozzi (2003) Hall et al. Productivity (g LÀ1 dÀ1) 1. tropical developing countries might be potential cultivation sites for commercial production of algal products. 2000). 1999.7 g LÀ1 dÀ1 (Carlozzi. 2003). the productivity reported was about 2. (2007).06 g LÀ1 dÀ1 (Garcı et al. J. in most tropical developing countries. Nevertheless. doi:10.. 1997. Ugwu et al. Chisti. outdoor cultures of algae can be maintained for relatively long period of time in a year because there is neither winter nor cold seasons in those regions. biomass productivities (in such systems) would depend on the prevailing weather conditions in a particular locality. E.R. In order to reduce the cost of producing algal biomass and products. (Camacho Rubio et al. there are seasonal variations in temperatures and solar light energy throughout the year in most of these regions...M.1016/j. Furthermore. which was used for cultivation of Nannochlorospis (Cheng-Wu et al.90 1.. geographical location.0 11 75 25.27 g LÀ1 dÀ1 was obtained in 440-L outdoor flat-plate photobioreactor.50 g LÀ1 dÀ1 was obtained ´ n Ferna ´ ndez et al. the increasing population and consequently. the biomass productivity ´ pez ´a-Malea Lo obtained was 0. Energy Convers.046 .000-L outdoor photobioreactor (developed for commercial production of astaxanthin from Haematococcus pluvialis). Large-scale outdoor photobioreactors should have large volume and occupy less land space. high-value metabolites should be produced to compromise the technical costs involved in algal production.01.05 g LÀ1 dÀ1 was obtained (Olaizola. 5. the exorbitant cost of land have attracted the attention of many scientists to look for alternative cultivation sites. Acie Molina Grima. In 200-L airlift tubular photobioreactor (which was used for outdoor cultivation of Phaeodactylum tricornutum). Manage. few large-scale photobioreactors with relatively good biomass productivities have been developed.20–1. Y..ARTICLE IN PRESS 6 C. with 200-L airlift-driven-tubular photobioreactor tested for outdoor cultivation of Phaeodactylum tricornutum. In 11-L undular row tubular photobioreactor (for Arthrospira platensis).000 55 440 Photosynthetic strain Porphyridium cruentum Phaeodactylum tricornutum Phaeodactylum tricornutum Chlorella sorokiniana Arthrospira platensis Phaeodactylum tricornutum Haematococcus pluvialis Haematococcus pluvialis Nannochloropsis sp. temperature. Sci.. 38. more efforts are still required to improve photobioreactor technologies and know-how of algal cultures. 2721–2732. It should be noted that for mass cultivation of algae. Benemann.G. biomass productivity of 1. Technol. be able to give high biomass yields.40 0.. Thus.47 2. The major issue in the design of efficient photobioreactors should be their capacity to maximize the outdoor solar radiation. biomass productivity of 1. Chem. about 0. one of the major steps that should be undertaken for efficient mass cultivation of algae. (2006) Garcı Cheng-Wu et al. Airlift-driven external loop tubular photobioreactors for outdoor production of microalgae: assessment of design and performance.20 1. References ´ n Ferna ´ ndez. Sa ´ nchez Pere ´ z. Although commercial cultivation of algae is done in developed countries. Bioresour. Eng. the target product. in 25. vast areas of land are required.90 g LÀ1 dÀ1 was attained (Molina et al. 56. 2001. Thus.. they should have transparent surfaces. Also. (2001) Ugwu et al. J. (1999) ´ n Ferna ´ ndez et al.70 1. (2003) Olaizola (2000) ´a-Malea Lo ´ pez et al. Table 3 shows the algal biomass productivities reported with different types and scales of outdoor photobioreactors. (2001) Acie Molina et al. Also. Acknowledgements The authors acknowledge the financial support provided to them by Japan Society for Promotion of Science (JSPS). as well as the overall cost of production. 475–479. Due to these problems. (2001) due to difficulty in maintaining optimum light..50 1.A.biortech. design and construction of any photobioreactor should depend on the type of strain. et al. and mass transfer in photobioreactors. photosynthetic efficiency or biomass yield (g-biomass per unit of solar radiation). It should be noted that aside from volumetric productivity (productivity per unit of reactor volume per unit of time) algal biomass productivity can be evaluated in photobioreactors based on areal productivity (productivity per unit of occupied-land area per unit of time). Conclusion and perspectives Despite that a great deal of work has been done to develop photobioreactors for algal cultures.2007.

G... Appl. P. Cysewski... Lee. 89–94.. 2006. Watanabe.. 1999... Morvan. M. Acie Camacho. 116. Morita. H.G. C. 2004. 157– 163. A laboratory scale airlift photobioreactor to increase biomass output rate of photosynthetic algal cultures.. 70... Mizoguchi. 157–167.. 2001... Bioresource Technol. Y. Rocking tray. 600. K.G.. Biosyt.G. TISTR 8208 in a seaweed-type bioreactor. H.M.. M. Chem... in a seaweed-type photobioreactor. 313–321. Liquid velocity and gas hold up in three-phase internal loop airlift reactors with low density particles.G. Y.046 .. Eng. A. 1988... 28. Appl...S.E. 1953. Takano. M. Technol.. Bioeng. Aquaculture 195.H. Maeda. Technol. Algal Biotechnology. Acie ´ n. L.. V. Biotechnol. J. Chetsumon.G. J.. ´a. Biotechnol. Grima. 452–455.L. TISTR 8208. 1331–1338. E. E. Pneumatically agitated bioreactors in industrial and environmental bioprocessing: hydrodynamics. J. 70. 98.. S. E. A pneumatically agitated flat-panel photobioreactor with gas recirculation: anaerobic photoheterotrophic cultivation of a purple nonsulfur bacterium. Rivas. A. tubes and fermenters. 1182–1189. Hu.. An industrialsize flat glass reactor for mass production of Nannochloropsis sp. London. Ferment. 1995. Energy. E. Chisti.. Lodeiro. K. In: Burlew. 113–118. Washington. M. Maeda. J... S.1016/j. 92.R. 1998. Antibiotic production by the immobilized cyanobacterium. 1988. ´ o Sa ´a-Malea Lo ´ pez. 1119–1126. Trosch... G. H. R. O. 1996.. 123. Proc. light availability and hydrodynamic stress in the growth of Phaeodactylum tricornutum in a concentric tube airlift photobioreactor.T. Young. Chatellier..Y... Bioeng. 1991.. Eng. Please cite this article in press as: Ugwu. T.F. Gudin. Wijffels. 98. 81. Sastre de Vincente.. Y.). E. A. (2007).L. Autotrophic growth and carotenoid production of Haematococcus pluvialis in a 30 liter airlift photobioreactor.. Effect of photobioreactor inclination on the biomass productivity of an outdoor algal culture. ´ n Ferna ´ ndez. 1998.. J.. Hall. Chisti. P. mass transfer. Prediction of dissolved oxygen and carbon dioxide concentration profiles in tubular photobioreactors for microalgal culture. Glutamate production from CO2 by marine cyanobacterium Synechococcus sp. 1999. Scaling up a tubular photobioreactor for continuous culture of Porphyridium cruentum – from laboratory to pilot plant. A flat inclined modular photobioreactor for outdoor mass cultivation of phototrophs. M. 35–49.B. Palsson. Biotechnol.. Molina Grima. Chaumont. Carnegie Institution.S. P. DC. Marvalin.. W. DC. 160–167.. ´ n Ferna ´ ndez. Shin. operation. Single cell protein production of Euglena gracilis and carbon dioxide fixation in an innovative photobioreactor.. J. Ferna 7 Molina Grima.A. Lee. N. 98. Acie Y. 51. 2003. 1991. Suh.G. J. Rodolfi.. S. Y. Couvert..C. M.. Technol. Washington.A. Algal Culture from Laboratory to Pilot Plant. A. E. Vandenberg. J.L. Powtongsook. M. Umeda. Oyama. Biotechnol. Zmora. Oikawa. T.. 305–315. Richmond. G. 43. Uebele. Guterman..G. Biotechnol. 539–543.. Del Rı ´ nchez. Dallaire.. H. Vonshak.. 1796–1803. Commercial production of microalgae: ponds. 322–329. J. M. Carlozzi. Biotechnol. p. 1991. Carnegie Institution of Washington. Milner.O. Bioeng. 2007.K. D. 2003. 2003. 2001. Prog. Bioproc. Photoautotrophic high-density cultivation of vegetative cells of Haematococcus pluvialis in airlift bioreactor. 51–60..J. 62–73. Hwang. hydraulic. Bioresour. 1990.M. Lu. Ferna ´ ndez Sevilla. B. Barriada.. Appl. Effect of algal incorporation on growth. F. and transport phenomena.. de la Nou ¨ e. B. in annular reactors. 1991. A. Ugwu et al. T. Merchuk. J.. E. Bioresource Technol. J. 1433–1439. C. Chetsumon. Bioresource Technol. How mixing enhances the photosynthetic production rate.. C. Outdoor helical tubular photobioreactors for microalgal production: modeling of fluid-dynamics and mass transfer and assessment of biomass productivity. 1381–1387. S. C. Hase. Bijmans. A. 2006. Photobioreactors: light regime. Verdus.. Biosci. No.J. Gluz. Garcı Interaction between CO2-mass transfer. Biotechnol.C. Commercial potential for Haematococcus microalgae as a natural source of astaxanthin. F. E. Tredici. and modeling of a membrane photobioreactor to study the growth of the cyanobacterium Arthrospira platensis in space conditions. Lee.. Choi. In: Stadler. Biosorption of cadmium by biomass of brown marine macroalgae. 1301–1310. High density photoautotrophic algal cultures: design. Comparison of photobioreactors for cultivation of the microalga Porphyridium sp. Cogne. 21. E. Evaluation of the marine algae Ulva fasciata and Sargassum sp. TIBTECH 18. J. Bioresource Technol. Tsavalos. 2002.. Hoekema.. Contreras.. Bioeng. Molina Grima. 97. T. 89. (Ed. Hydrodynamic and mass transfer study in a rectangular three-phase airlift loop reactor. S. R.. 331–335. 247–253. Garcı ´a Camacho Rubio. Sasao..O. P.. Bosca. 2000. Richmond.. 113–131. 1996. construction and operation of a novel photobioreactor system. M. 199–208. New phytol. Aquaculture 72. tanks. J.. M. 79. 231–247.. 15.. J. Bioeng. A. 107–114. D.. Shotipruk. Garcı 2006. Richmond. F. Comparative analysis of the outdoor culture of Haematococcus pluvialis in tubular and bubble column photobioreactors.. Y. F. Thepenier... A novel airlift photobioreactor with baffles fro improved light utilization through flashing light effect. P.J. Enzyme Microb. Biotechnol. R. Photosynthetic production of microalgal biomass in a raceway system under greenhouse conditions in Sendai City. 2007. 357.R..... Cheng-Wu. 6. R. Lessard. Matsunaga. Chini Zittelli.. Biotechnol. E. survival and carcass composition of rainbow trout (Oncorhynchus mykiss) fry. Chem... Boussiba. F. N. 185–188.. Biotechnol. Biotechnol. R. 50. Biotechnol. J.. Degen. I. M..P... Acie ´n Garcı ´ ndez. Janssen.. K. Z. Burlew. Dauta.. Balasubramanian.... Sode. Takeyama.. Bioresource Technol.A.. Molina Grima. 249–256. Schmidt-Staigar. Lorenz. Sci. Garcı ´a Camacho. J. Lee.. Y.. 2005. I. 257– 263.S. Mazzuca Sobczuk. (Eds... Cornet. 96. C. Chisti. F. 318– 325.U. 38. D. Phycol. H. Kopel. J. H. 2005. Karthikeyan.. 329–342. 2000..J. 51. Chae. Yagi.. Christiaen. M. BenAmotz. J.. Chang. S. 243–250. Shelef. 2003. M. I. Biotechnol. Miura. p.. K.C. Low. Biochem. F. Bioresource Technol. G. 82.. pp.. Kaewpintong..... Yagi. A.M. / Bioresource Technology xxx (2007) xxx–xxx Borowitzka. Sa ´ nchez Pe ´ rez. 1994.S.. E. Hirano. (Eustigmatophyceae). Sandbank. Umeda... Z. Dilution of solar radiation through culture lamination in photobioreactor rows facing south–north: a way to improve the efficiency of light utilization by cyanobacteria (Arthrospira platensis).. 403–409. Y. Elsevier Applied Science. Cordero. Morillon.S.. Mech. and scale up. 1999. Bioeng. 92. J. 2001. Rao. J. et al. A. Hydro. B. T. S. Photobioreactors for mass cultivation of algae. Broad spectrum and mode of action of an antibiotic produced by Scytonema sp. Bioeng 62. Eng. 38.. 75. J. G. 995–1000. 108. Chisti. doi:10. I. F. for the biosorption of Cu(II) from aqueous solutions. Lumostatic operation of bubble column photobioreactors for Haematococcus pluvialis cultures using a specific light uptake rate as a control parameter. C. using a novel biosolar reactor employing light diffusing optical fibers. A. Janvanmardian. 38.K. D. C. Tubular Molina. Appl. C. Bioeng. Retze. Miura. Appl.R.01.C. J.. J. M. A. G. Harker. 1998. Bastoul... Rev. F.. J. C... A. C. Roustan.J.. Q. Molina Grima. Mizoguchi. Light emitting diode-based algal photobioreactor with external gas exchange.. 33–112.. A..J. Phycol.S.. Ferment... Ariura.G. 27. 741–750.. Palsson. (28/29).S. Algal Culture from Laboratory to Pilot Plant. F. W.. Pavasant... H.. H. Biochem. O.2007. Biotechnol. Ferna photobioreactor design for algal cultures.T. 60. Biotechnol.U. M. Casas Lo ´ pez. Herrero.). Mukmenev. 33. J. F. J.Ø. Hwang. ´a Camacho.. Outdoor cultivation of the marine microalga Isochrysis galbana in open reactors.. K. Karamanos. 82. Chem.A. 1953.biortech. S. Gross.ARTICLE IN PRESS C.W. 1995. Merchuk.. Intensive outdoor algal cultures. Biotechnol.. 70–72. Scytonema sp. Cohen.. Mass cultivation of Nannochloropsis sp.. 2007. Guerrero. Fernandez.. Burgess.. J. 71–86. J.. A.... Arad. Guerrero. S. Nakamura. Bioeng. Sudo. Int. 2000... F... ´ ndez. Bioeng. Iyer.. J.. U. A.. R. W. Design.. Tramper. Effects of agitation on the microalgae Phaeodactylum tricornutum and Porphyridium cruentum. 288–295.. Bazin.

15. Liu.U. Tanaka.C. R.. Boussiba. J.. 331–345. Pottier. 31–35. Appl. G. Choi. Pruvost.. Y. Manage.O. S. Miyachi...S. P. Tanaka. H. Karamanos. An integrated solar and artificial light system for internal illumination of photobioreactors. H. pp. Ugwu... H. J. Ogbonna. 33B. Appl. Photobioreactor design for photobiological production of hydrogen..biortech. Eng. J. Tanaka. 1992. Materassi. 58. Design of static mixers for inclined tubular photobioreactors. A. H.. C.R. 58. Pavasant. A. 1999. E.. Eng. Proc.). Sung. Algal Biotechnology. Phycol. 499–503. (Eds. 1986.. Tanaka. Handbook of Microalgal Culture. London. Zhang.. J.R... New York.ARTICLE IN PRESS 8 C. J. pp. Ichige. (Ed.. 31.. 2000. A. Appl. E. 1985. J. Chem. J. 92. H. C. Biotechnol. T.. 61–74. 6430–6437. Oswald. A.C. Eng. Golueke. 2000.. Improvement of mass transfer characteristics and productivities of inclined tubular photobioreactors by installation of internal static mixers. Lee.. Adv.. Vonshak..J.. Morvan. Adv. Multistage continuous cultivation of bluegreen alga Spirulina maxima in the flat tank photobioreactors. 1986. Tredici. Photobioreactors for the axenic mass cultivation of microalgae. Wilde. Biochem. H. 35–38. Biotechnol.046 . Ramos de Ortega.W. Dominı A.. A new tubular reactor for mass production of microalgae outdoors. Ogbonna. C. M. R. Bioresource Technol. 47. Production of Spirulina biomass in closed photobioreactors. J. Y.. et al. Tanaka.. A tubular photobioreactor for photosynthetic production of biomass from carbon dioxide: design and performance. Microbiol. Olaizola.R. 527–534.. (2007). Biotechnol. 187–197.. W. 2002... Bocci.C. Mass transfer from Taylor bubbles rising in single capillaries.. Y. Appl. M. Bioeng.J. G. Lett.). Chem. Ugwu.U. 791–799. 3406–3411. ´ gues-Bocanegra. Biotechnol. 60. Tanaka.. S. K. 38. Ogbonna.J.U.. M. Biohydrogen. Krishna. J. 2003.. Microbiol. Efficiency of sunlight utilization: tubular versus flat photobioreactors. S. 2005a. J. Pirt. Christiaen. 11. Kopel. Ogbonna. Biotechnol. R. Muller-Feuga. 1998. M. C. Y.. J. T. J. R. M.. Wongsuchoto. 75–78. T. Saiki. Balyuzi. Elsevier Applied Science. 327–332... P. 2004. Biotechnol. H. 600–607. 2002. Shin. Legrand. Ogbonna..D. Plenum Press.. Kondo. Park. Matsunaga. Bioeng. F.. Growth and characterization of microalgal biomass produced in bubble column and airlift photobioreactors: studies in fed-batch culture. Technol. S. 2005b. P.. Florenzano. Phycol. C. San Pietro. Bioeng. 1993.. 12.R. Samson.C. Ugwu...G. 289–297.C..R.. 68.. Pushparaj. 441–451. Numerical investigation of hydrodynamic and mixing conditions in a torus photobioreactor.. G. 68.). J. Microbiol...C. Haematococcus pluvialis cultivation in split-cylinder internal-loop airlift photobioreactor under aeration conditions avoiding cell damage. Blackwell Publishers. 221–231. Please cite this article in press as: Ugwu. Garcı ´a Camacho. Phycol.. 2001.1016/j. J.. Ogbonna. 532– 538.. Invention of outdoor closed type photobioreactor for microalgae. T.U. Vega-Estrada. J.. Charinpanitkul. Commercial production of astaxanthin from Haematococcus pluvialis using 25.W. H. A. F. Biomass 11. Biosys. Pergamon Press. Torzillo..U. J... Materassi.R. 209–217. 1960. Appl. Verdus.. Balloni. Optimized aeration by carbon dioxide gas for microalgal production and mass transfer characterization in a vertical flat-plate photobioreactor. Tsuchiya. M. Environmental stress physiology. pp. 1999.J. Martin. C. Interactions between photoautotrophic and heterotrophic metabolism in photoheterotrophic cultures of Euglena gracilis. doi:10. 15. (Eds. Eng.. 4476–4489. J. Lee. J. In: Miyake. H.K.C. 1015–1023. 329–343. Phycol. Cero ´ n Garcı ´a. Microalgal biotechnology at the turn of the millennium: a personal view.H.C. 105–112.. Pohl.. Ugwu et al. 27. Light/dark cyclic movement of algal cells in inclined tubular photobioreactors with internal static mixers for efficient production of biomass. A.C.. 1998.. Sci 61. Enzyme Microb. 141–156. Watanabe. E.. Vandu. Microbiol.U. Bubble size distribution and gas–liquid mass transfer in airlift contactors. A. 2. 70. Tredici. Chisti... Ogbonna. Appl. Photobioreactors for mass cultivation of algae. Symp. pp. Oxford. 63. Tanaka. 245–261. M. In: Zaborosky. G. Biotechnol. 1997. Phycol. M.. M. K.2007. CO2 fixation by Chlorella sp. A. Chini Zittelli.. 2000... / Bioresource Technology xxx (2007) xxx–xxx Sato.C. Chem. Biological transformation of solar energy. Tanaka. J.. Development of efficient large scale photobioreactors. J. 2006. Bioremoval of heavy metals by the use microalgae. Montes-Horcasitas. (Ed. D. J. 223–262.C. H.. J. ´ nchez Miron.. Energy Convers.. 97–101. S. 2005.. In: Stadler. T. 2006. Roux. Biohygrogen II – An Approach to Environmentally Acceptable Technology. Appl. Soejima. M. Vonshak. 2003. Mollion.. Biotechnol. Molina Sa Grima. Tech. W. Technol. 57–82. M.000-liter outdoor photobioreactors. H. Appl.. 4..... Chem. H... 269–273. L. Ogbonna. Chem. 781–812. Characterization of light utilization and biomass yields of Chlorella sorokiniana in inclined outdoor tubular photobioreactors equipped with static mixers. J.. KR-1 and its cultural characteristics. B. Sci. Richmond. 2005. 40. K. A. M. Bioproc. 1985. Appl. R.. Appl. 5. N. Phycol. O. C. Kohlhase. Walach.. Soejima. 81–90. Kurano. Y.. T.01. Bioresour.. 1983. Energy Convers.). 25. Torzillo. J. Benemann.C. 2002. From open ponds to vertical alveolar panels: the Italian experience in the development of reactors for the mass cultivation of photoautotrophic microorganisms. C. In: Richmond. 1993..... Manage. Pirt.. for removal of CO2 in stack gas. A...M. Can ˜ izares-Villanueva. Ugwu. The role of microalgae in aquaculture: situation and trends. 1988. Production of Chlorella biomass in different types of flat bioreactors in temperate zones. 12.O... Y.. London and New York. Biotechnol. 217–223. Development of photobioreactor incorporating Chlorella sp.. J. Can. 57. Photoautotrophic bioreactor using visible solar rays condensed by fresnel lenses and transmitted through optical fibers. 12. Bazin. 499–506. Leduy.. 2002.S. R. Mori.C. J. Usui. Richmond. Biomass 10.

Sign up to vote on this title
UsefulNot useful