3516

Ind. Eng. Chem. Res. 2010, 49, 35163526

Photobioreactor Design for Commercial Biofuel Production from Microalgae

Aditya M. Kunjapur* and R. Bruce Eldridge
Process Science and Technology Center, UniVersity of Texas, Austin, Texas 78712

This review paper describes systems used to cultivate microalgae for biofuel production. It addresses general design considerations pertaining to reactors that use natural light and photosynthetic growth mechanisms, with an emphasis on large-scale reactors. Important design aspects include lighting, mixing, water consumption, CO2 consumption, O2 removal, nutrient supply, temperature, and pH. Though open pond reactors are the most affordable option, they provide insufcient control of nearly all growth conditions. In contrast, a variety of closed reactors offer substantial control, but few feature the likelihood for levels of productivity that offset their high cost. One of the greatest challenges of closed photobioreactor design is how to increase reactor size in order to benet from economy of scale and produce meaningful quantities of biofuel. This paper also highlights the concept of combining open and closed systems and concludes with a discussion regarding a possible optimal reactor conguration.
1. Introduction Many strains of photosynthetic microalgae produce lipids that can be converted into various types of biofuel, such as biodiesel or jet fuel.1 The potential of using photosynthetic microalgae to produce biofuel is of particular interest at this time. Americas deepening dependence on foreign sources of petroleum-based fuel jeopardizes the national economy and national security. Increasing CO2 emissions may promote climate change. Rising demand for energy from developing nations threatens the availability of sustainable energy for future generations. Commercial biofuel production using algae could mitigate all of these issues: algae can be cultivated in the United States, algae consume CO2 during photosynthesis (ideally resulting in a carbon neutral fuel), and increased biofuel production would supplement nonrenewable energy sources.2 Microalgae are already produced commercially for a variety of other applications, which include human nutrition, animal feed, aquaculture, pigments, and cosmetics.3 Algae can also be cultivated using photoautotrophic (or photosynthetic), heterotrophic, or mixotrophic growth techniques. Heterotrophic growth is based on the cellular consumption of organic carbon instead of light, and mixtrophic growth uses the combination of these energy sources. Although some authors, such as Lee,4 have discussed advantages of heterotrophic and mixotrophic growth, these methods are not described here. As Chisti noted, heterotrophic growth mechanisms are not as efcient as photosynthetic growth mechanisms because the carbon source used to feed the algae was ultimately derived from another plant by photosynthesis. In addition, the carbon source may compete with food sources for human consumption.5 Henceforth, the generic term algae will be used to describe photosynthetic microalgae and the term photobioreactor will be used to describe a system that uses light to grow algae via only the photosynthetic mode of cultivation. Algae can be grown with exposure to natural or articial light. Articial lighting techniques have provided insight into how algae respond to varying light conditions, and these insights are briey discussed in the design considerations section of this paper. However, this paper does not focus on growth systems that rely on articial lighting because of energy efciency
* To whom correspondence should be addressed. Tel.: (713)-7025587. Fax: (512)-471-1720. E-mail: aditya.kunjapur@mail.utexas.edu.

considerations. The energy used to power the articial lighting was once derived from sunlight. This energy necessarily experienced losses along every stage of its transformation to and from electrical energy, and these losses are not incurred by natural light. The two major classes of algae growth systems are open ponds and closed reactors. However, prior to the analysis of specic photobioreactor congurations, general design considerations are presented so that reactor designs can be evaluated and compared effectively. During the description of these factors, individual reactor types may be mentioned in order to better explain the design aspect. Following the discussion of design considerations, these reactor types will be discussed in detail. 2. Photobioreactor Design Considerations Numerous aspects inuence the growth and lipid content of algae. The reaction driving the initial conversion of sunlight into stored energy is photosynthesis. Therefore, all of the components involved in photosynthesis contribute to growth. The factors discussed in this paper are lighting, mixing, water, CO2, O2 removal, nutrient supply, temperature, and pH. The list is not comprehensive, and the nal topic within this section addresses other critical issues, such as genetic engineering and reactor maintenance. It is important to note that in each category the precise conditions for optimal growth depend on the strain of algae selected for cultivation. 2.1. Lighting. An optimal reactor enhances light intensity/ penetration, as well as the wavelength of light and the frequency of cellular exposure to light. The level of light intensity is critical because at a certain level algae experience light saturation and dissipate the excess energy as heat.6 Light saturation can be mitigated by the spatial dilution of light, which is the distribution of solar radiation on a greater photosynthetic surface area. Spatial dilution of light also reduces mutual shading of cells in the culture, which results in higher growth rates and lower content of accessory pigments.7 Thus, a design principle for photobioreactor designs is to maximize the surface area to volume ratio, which can be used for comparison between reactors. Designs resulting in a ratio value of 400 m2/m3 were state-of-the-art in the year 2008.8 Beyond the surface area and volume, the unique geometry of a reactor inuences the light distribution. In a tubular reactor, for

10.1021/ie901459u 2010 American Chemical Society Published on Web 03/23/2010

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3517

Figure 1. Rectangular airlift reactor with separate light collection. (Reprinted with kind permission from ref 9. Copyright 2003 John Wiley and Sons.)

example, the light gradient is primarily determined by the diameter of the tube and the biomass density in the medium.9 The biomass density affects both the light intensity and the light penetration. Optimal cell density is specic to each strain and needs to be maintained in order for light intensity and light penetration to remain at optimal levels.10 Park and Lee described an important operating parameter known as the critical cell density, which is the maximum cell concentration without mutual shading in algal cultures.11 The wavelength of light used to cultivate algae is also a design factor because some experiments have shown that cultures grow differently when exposed to different colors of light. However, optimizing this aspect in systems illuminated by natural light is much more challenging than in systems illuminated by articial light, where the wavelength of light shone can be selected. Unfortunately, more than 50% of the incident solar radiation from natural light cannot be used by photosynthesis.12 When natural light is the growth rate limiting factor, the upper limit in the light conversion efciency of a large-scale culture may result in a maximum potential yield of 30-40 g/m2 d.13 Matthijs et al. found that red light matched perfectly with the requirements of the rst excited state of pigments present in the light-harvesting antenna complexes (LHC) central to photosynthesis in green algae. He also noted that the addition of blue light to the red LED light did not change the growth properties.14 Light and dark cycles strongly inuence the growth of algae. In both open ponds and outdoor closed reactors, natural light is subject to changes in time of day, weather, season, and geography.12 Unfortunately, all reactors using natural light are subject to the absence of light during nighttime. According to Chisti, biomass losses might reach as high as 25% during the night, depending on the light intensity during the day, the temperature during the day, and the temperature at night.5 Janssen et al. noted that the length of the light/dark cycles experienced by algae inuenced photosynthetic efciency. Cycles on the order of milliseconds increased the photosynthetic efciency (PE) of Dunaliella tertiolecta, but cycles on the order of seconds lowered the PE compared to continuous lighting.15 The time length of the dark reactions in photosynthesis may serve as the rate-limiting step for photosynthesis and growth in

general.16 The optimal dark period depends on the photon ux density of the previous light period and the uid residence time in zones of different irradiance.17 Formulas that describe light and dark frequency values in various types of closed reactors can be found in the literature.9 Such formulas and other quantitative models for light analysis are not included in order to maintain brevity. Likewise, predictive equations that model mass transfer or other design parameters are excluded here but can be found in referenced papers. The combination of factors such as the length of the light and dark cycles and the light intensity result in the overall light regime in a photobioreactor. Light regime strongly inuences photoacclimation, which describes the physiological responses of cells to rapid changes in light intensity. An example of a common response to light intensity alteration is a change in chlorophyll pigment content. However, a sudden surge of light can be fatal for many species of algae.18 Thus, it is important to consider light regime and photoacclimation when designing a reactor, particularly in order to maximize the photosynthetic efciency. Because light is the exclusive source of energy in the photosynthetic mode of cultivation, an important calculation can be performed if solar radiation per area data is available for the location of cultivation. On the basis of this data and other values such as photosynthetic efciency, the maximum theoretical oil yield per area can be determined. The maximum theoretical oil yield per area is especially useful for comparison between actual and ideal reactor performance when the oil yield and area of a reactor in operation are known. However, reactor area does not directly contribute to oil yield when light is collected externally from the site of algal cultivation, which some authors have advocated.9 Figure 1 depicts a rectangular reactor that collects light externally. Experiments conducted by Feuermann et al.19 and Zijffers et al.20 suggested that natural light can efciently be collected at a separate location and delivered to a photobioreactor using ber optic cables. Zijffers et al. employed the light guide technology in a at-plate reactor known as the Green Solar Collector.20 The schematic of this reactor is shown in Figure 2. In such a design, light must enter the light guides and experience total internal reection. It must also refract out of the guide when surrounded by the algal suspension. In order to

3518

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 2. Cross-section of the photobioreactor (Green Solar Collector). The numbers indicate the following: 1: linear Fresnel lens, 2: light guide, 3: at-panel reactor compartment, 4: perforated tube for aeration, 5: water jacket. The letters indicate the following: A: legs holding the lens, X: axis of rotation of the lens, Y: axis of rotation of the legs A.20 (Reprinted with kind permission from ref 20. Copyright 2008 Springer Science + Business Media.)

achieve this, a light guide surrounded by air and accepting all possible angles on the top surface must have a refractive index higher than 1.415. Polymethylmethacrylate (PMMA) is recommended as an ideal material for this application. The light guide should be at at the top surface of the entrance and triangular at the bottom surface within the reactor in order to ensure that maximal light enters and leaves the guide respectively. Light intensity is then determined by the ratio of the surface of the lens to the surface of the light guide in the reactor.20 Light-emitting diodes (LEDs) have been used frequently in the literature as the sole light source for many photobioreactors. Because much of the LED literature has provided insight into light effects in general, some results of algae grown using articial lighting systems will be discussed. Matthijs et al. found that the use of ashing LEDs in indoor algal culture yielded a major gain in energy economy compared to luminescent light sources.14 Gordon and Polle16 advocated a lighting technique using LEDs that pulsed on the order of tens to hundreds of microseconds while also increasing the instantaneous photonic ux. The authors noted that though ashing of light might not always improve productivity, optimal pulsing could dramatically improve productivity. The use of LEDs to produce a ashing light will increase operating costs, but the authors claimed that the costs could be offset by greater increases in productivity.16 Although much of the literature supports the ashing light effect, some authors have cautioned against accepting it. Pulz and Scheibenbogen12 cited some experiments that may leave the effect of ashing light inconclusive. However, it is possible that in these experiments the light was not ashing at a frequency within the effective range. 2.2. Mixing. The level of mixing in a reactor strongly contributes to the growth of algae. In fact, Suh and Lee stated that when environmental conditions do not limit growth rates, mixing is the most inuential factor contributing to algae growth rates.21 Mixing affects growth in two primary ways. Mixing improves productivity by increasing the frequency of cell exposure to light and dark volumes of the reactor and by increasing mass transfer between the nutrients and cells.22 Mixing attempts to distribute radiation evenly to all cells in the culture and reduce diffusion barriers around the cells.10

Figure 3. A. Dual sparging photobioreactor with CO2 additions separated from ow of air for mixing: a, culture outlet; b, air outlet through condenser; c, medium inlet; d, medium reservoir; e, glass cylinder; f, pH electrode; g, automatic titration device; h, solenoid valve; i, perforated membrane sparger; j, air pump; k, orice sparger; l, light tubes; m, mirror; n, air lter. B. Bottom part of photobioreactor operated as ordinary bubble column with CO2 mixed with ow of air formixing. Annotations as in A. C. Bottom part of photobioreactor operated in stirred bioreactor conguration. CO2 is mixed with ow of air for mixing: o, impeller; other annotations as in A.25 (Reprinted with kind permission from ref 25. Copyright 1998 Springer Science + Business Media.)

Mixing and lighting are closely related, as mixing is often responsible for inducing the light and dark cycles benecial to algae growth. Similarly, mixing offers little benet if lighting is poor. The signicance of this relationship was veried by Richmond, who described that the rate of mixing did not affect productivity when cultures were exposed to low light and low cell density.10 Ugwu et al. demonstrated that the installation of static mixers in tubular reactors succeeded in increasing light utilization and biomass yields when the reactor was scaled up by increasing the tube diameter.23 A review by Ugwu et al.24 listed some of the factors that inuence the overall mass transfer coefcient (kLa) in a reactor, which is a key comparison parameter between reactors. The coefcient depends on the agitation rate, type of sparger, surfactants/antifoam agents, and temperature. The use of ne spargers could result in the formation of large bubbles, which leads to poor mass transfer because of the reduced contact area between liquid and gas. The size of the bubbles and the gas bubble velocity are dependent on the liquid ow rate. Bubble size may be reduced with the installation of static mixers or bafes.24 Eriksen et al. described a closed reactor with a dual orice and perforated membrane sparger system which separates the CO2 supply from the air supply used for mixing.25 Figure 3 displays the experimental apparatus. This separation resulted in ve times the magnitude of transfer of CO2 from gas phase to liquid phase relative to conventional sparging. Eriksen et al. described many advantages achieved by combining two types of spargers in the dual sparging bioreactor. First, the small size of the bubbles from the membrane sparger increased the CO2 mass transfer coefcient. Second, the separate addition of CO2 also improved mass transfer by increasing the gradient of CO2 partial pressure between the liquid and gas phase. Third, the large air bubbles generated turbulence that reduced wall growth. The dual sparging bioreactor also displayed a high degree of reliability since there were no equipment failures and limited maintenance was required.25 According to a review by

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3519

Janssen et al., sparger design does not effectively increase mixing in bubble-column reactors, but spargers can improve air-lift reactors if applied to the annulus rather than the inner cylinder. The level of mixing has to be optimized carefully because high levels of mixing will result in cell death from shear. Barbosa et al. found that bubble formation is the main cause for cell death in gas-sparged reactors, and gas entrance velocity could be used as a measure for estimating cell damage in these reactors. Surprisingly, bubble bursting and bubble rising were proven not to contribute to cell death. Barbosa et al. recommended keeping the gas velocity at the sparger lower than the critical value by increasing the number of nozzles and/or increasing the nozzle diameter in order to minimize shear-related cell death.26 2.3. Water Consumption. A noteworthy benet of producing fuel from many strains of algae, as opposed to conventional crops, is that the cultivation does not have to require freshwater. Water supplies, particularly freshwater supplies, are under pressure in many parts of the globe, and greater biofuel production places an additional burden on those supplies.27 Thus, water consumption is a key comparison parameter among reactor options. Wogan28 mentioned that algae can grow in a much wider range of water sources than other terrestrial crops. Studies have shown that algae can grow in fresh drinking water, saline or brackish water, and even wastewater efuent.29 Strains of microalgae are generally divided into two categories based on whether they grow optimally in freshwater or saltwater. The level of salinity inuences the overall productivity as well as individual production rates of lipids and carbohydrates in each strain of algae.30 A few examples of strains and their optimum salinity values are included to provide a sense of how saline the growth media can be. Abu-Rezq et al. found optimum production conditions for species of Nannochloropsis, Tetraselmis, and Isochrysis. The optimum salinity range was 20-40 ppt for Nannochloropsis, 20-35 ppt for Tetraselmis, and 25-35 ppt for Isochrysis.31 As mentioned earlier, wastewater can be used to cultivate algae. Using wastewater for this application provides two signicant benets: algae receive an inexpensive medium rich in required nutrients and the wastewater is further treated in the process.28 Wastewater efuent generally contains high concentrations of nitrogen and phosphorus, and unwanted algae growth and eutrophication occur when other water bodies receive the efuent. The nitrogen and phosphorus concentrations can instead be minimized by passing the wastewater through an algal reactor.32 A major disadvantage of open ponds is the loss of water to the atmosphere by evaporation.8 When water evaporates from the reactor, the concentrations of all species present increases, and this can be a particular problem with saltwater ponds as the salinity could rise above tolerable values. 2.4. CO2 Consumption. In addition to light and water, carbon dioxide is necessary for photosynthesis to occur. However, an excess of CO2 can also be detrimental to photosynthesis and cell growth. Lee and Tay33 found that Chlorella cells exposed to high CO2 partial pressures (pCO2) experienced declining growth rates. CO2 can be supplied via diffusion through a gas permeable membrane in order to provide sufcient CO2 to the entire culture while preventing CO2 inhibition at high gaseous pCO2.33 CO2 concentrations from 1% to 5% (by volume) often lead to maximum growth. Despite this, laboratories routinely aerate algal cultures with 5-15% CO2, or even

Figure 4. Tubular reactor equipped with airlift system. (Reprinted with kind permission from ref 36. Copyright 2001 Elsevier.)

pure CO2.21 In the review by Schenk et al.,8 it was stated that a pCO2 value of at least 0.15 kPa is required to prevent kinetic CO2 uptake limitation. In addition, a ratio of about 1.7-1.8 g CO2/g dry biomass is required.5,8 Flue gas is a desirable source of CO2 because it reduces greenhouse gas emissions as well as the cost of algal biofuel production.34 Flue gas from typical coal-red power plants contain up to 13% CO2.5 Doucha et al.34 studied the performance of a closed reactor utilizing ue gas as a source of CO2 versus a reactor utilizing pure CO2. An infrared-analyzer that measures the bypass concentration of CO2 in the gas phase can be used to regulate the ow rate of ue gas. A pCO2 higher than 0.1 kPa was maintained at the downstream end of the reactor in order to prevent growth limitation by CO2. Surprisingly, productivities and photosynthetic efciencies were very similar under conditions of pure CO2 versus ue gas. Because CO2 concentration in ue gas was relatively low, the efciency of CO2 mass transfer was lower for ue gas than it was for pure CO2. In addition, the authors found that the presence of NOx and CO in ue gas did not inhibit the growth of microalgae.34 The cost of CO2 has to be considered when evaluating the economics of biofuel production from microalgae. A review by Carvalho et al.35 suggested that because supplying CO2 continuously is expensive, it may be necessary to supply it discontinuously. The authors recommended using hollow-ber membranes, which may improve mass transfer and reduce costs.35 2.5. O2 Removal. A high presence of oxygen around algae cells is undesirable. The combination of intense sunlight and high oxygen concentration results in photooxidative damage to algal cells.5 As a general guideline, oxygen concentrations should be maintained below 400% of air saturation value.5 Because oxygen does not build up substantially in open ponds, this is one aspect in which open ponds perform better than closed reactors. Because of the constraint on the concentration of dissolved oxygen, tube length is limited in horizontal tubular reactors. This restriction makes it very difcult for tubular reactors to be scaled-up. In a tubular reactor designed by Molina et al., the algae culture regularly returned to an airlift zone where the accumulated oxygen from photosynthesis was stripped by air. A gas-liquid separator in the upper part of the airlift column prevented gas bubbles from recirculating into the horizontal loop of the airlift reactor.36 Figure 4 is an illustration of the photobioreactor conguration used.

3520

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

The time taken by the uid to travel the length of the degasser must at least equal the time required by the oxygen bubbles to rise out.36 If practical, the capture and sale of this oxygen stripped from the reactors may be an opportunity to reduce the cost of biofuel production. 2.6. Nutrient Supply. In order to grow, algae require more than the reactants in the photosynthesis reaction. Two major nutrients are nitrogen and phosphorus, which both play a role in controlling growth rates and lipid production. Other essential nutrients are carbon, hydrogen, oxygen, sulfur, calcium, magnesium, sodium, potassium, and chlorine. Nutrients needed in minute quantities include iron, boron, manganese, copper, molybdenum, vanadium, cobalt, nickel, silicon, and selenium.21 An analysis of a common medium known as N-8 revealed the deciency of iron, magnesium, sulfur, and nitrogen at high cell concentrations. Additional experiments showed that the separate addition of each of the four elements did not improve culture performance, but that balanced supplementation resulted in improved performance. The experimenters therefore asserted that balancing the nutrients based on the elemental composition of the biomass should be the basis for effective medium design.37 However, Chisti noted that some nutrients need to be present in excess. For example, phosphorus must be supplied in excess because the phosphates react with metal ions.5 Applying stress in the form of limited nutrients (especially N or P) can increase lipid percentages within the biomass. However, this stress application also curtails the growth rate and thus may lower overall lipid production. The trade-off between productivity and lipid content stems from the high metabolic cost of lipid biosynthesis. Rodol et al. described three different situations of nutrient supply: nutrient-sufcient, nutrient-limited, and nutrient-decient. The rst case should be evident, but the difference between the latter two cases may be subtle. Nutrient limitation occurs when cells are grown in an environment of a constant, but insufcient, supply of a limiting nutrient, to which the cells generally adapt. Nutrient deciency is characterized by the cultures reliance on endogenous reserves because there are no nutrients in the environment. Rodol et al. compared the growth of a few robust strains under all three conditions, with the nutrient-decient scenario applied to microalgae previously grown in a nutrient-sufcient environment. The authors found that the genus Nannochloropsis was an exception to the rule and had both enhanced lipid content and lipid productivity in an N-decient environment.38 2.7. Temperature. Temperatures experienced by algae grown outdoors can vary as much as the extreme outdoor temperatures characteristic to the geographic region of cultivation. Although algae may be able to grow at a variety of temperatures, optimal growth is limited to a narrow range specic to each strain. For example, Abu-Rezq et al. found that the optimum temperature range for Nannochloropsis, Tetraselmis, and Isochrysis was 19-21, 19-21, and 24-26 C, respectively.31 Seasonal and even daily uctuations in temperature can interfere with algae production. Temperatures can reach as high as 30 C higher than ambient temperature in a closed photobioreactor without temperature control equipment.21 Evaporate cooling or shading techniques are employed frequently to inhibit temperatures of that magnitude. In addition, a lower temperature appears to reduce the loss of biomass due to respiration during the night.5 2.8. pH. Each strain of algae also has a narrow optimal range of pH. The pH of the medium is linked to the concentration of CO2. Suh and Lee21 mentioned that pH increases steadily in the medium as CO2 is consumed during ow downstream in a

reactor. The pH affects the liquid chemistry of polar compounds and the availability of nutrients such as iron, organic acids, and even CO2.39,40 Because pH is so inuential, Suh and Lee stated that commercial pH controllers must be used in reactors to optimize growth.21 2.9. Other Considerations. Tredici and Zittelli asserted that a sustainable production process, which relies on a homogeneous and stable environment for microalgae cells, is more important in industrial applications than high yields.7 When evaluating a proposed reactor conguration, it is important to consider the production process as a whole. For instance, a major advantage of high cellular lipid content is the improved efciency of oil extraction and other downstream processing.38 The ease of integration of the reactor design with downstream processes is another key comparison parameter to reect upon. Techniques rooted in biology, rather than reactor design, can have a dramatic impact on the economics of algae production. Chisti suggested that genetic engineering may have the greatest likelihood of improving the economics of biofuel production from microalgae.5 Genetic engineering could enhance fuel production in a variety of ways, including improving photosynthetic efciency, increasing biomass productivity, increasing cellular lipid content, and improving temperature tolerance of algae to reduce cooling expenses.41 In addition, genetic engineering could increase algal cells tolerance to light saturation, photoinhibition, and photooxidation.5 Rodol et al. mentioned that a strain should be highly productive in outdoor culture and adaptable to the varying conditions of an outdoor environment. The authors asserted that there may be many suitable strains of microalgae among the thousands of natural strains available, and that for immediate purposes, there is no need to genetically modify microalgae. Genetic engineering can improve productivity and economics, but it will require long-term research and funding, as well as overcoming regulations against the release of genetically modied organisms.38 In addition, Pulz and Gross presented several reasons to be wary of genetic engineering. First, the authors claimed that increases in lipid content and other valuable cellular components are inherently constrained by cellular metabolism. Second, genetically modied algae may have a variety of detrimental effects on the environment. Finally, Pulz and Gross argued that genetically modied algae are not as t as natural strains and thus unlikely to overcome competition without the aid of other agents.42 Nevertheless, genetic engineering has tremendous potential and has already achieved successes in the laboratory. For example, Mussgnug et al.6 described experiments that altered the light harvesting complexes (LHCs), which were mentioned earlier in the Lighting section. The purpose of the LHCs is to capture solar energy and control the ow of the excitation energy to the photosynthetic reaction centers. They also facilitate the dissipation of light energy as heat or uorescence when irradiation exceeds photosynthetic capacity. This second trait is especially undesirable in algal bioreactors because it reduces efciency. To resolve this issue, the authors used RNAi technology to create a mutant of C. reinhardtii (referred to as Stm3LR3) that signicantly down regulated the amount of LHCI and LHCII complexes. Their experiments, which were successful, also showed that the reduction was permanent, something that had not previously been reported in literature. The strain of Stm3LR3 resulted in a decrease in dissipation of captured light energy, an increase in photosynthetic quantum yield, and reduced sensitivity of the system to photoinhibition. Further-

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3521

Figure 5. Schematic of a raceway pond. (Reprinted with kind permission from ref 5. Copyright 2007 Elsevier.)

more, despite the reductions in the LHC proteins, the remaining pigments were sufcient to drive photosynthesis efciently and promoted increased cell growth and replication compared to the parent strain at elevated light conditions. The use of down regulated LHC strains of algae is expected to result in a myriad of benets for algae production: reduction in energy losses, increase in overall photosynthetic efciency, improvement in light penetration, increase in the optimally illuminated cell proportion, and an increase in overall productivity.6 Geography also plays a role in reactor selection and assessing the feasibility of biofuel production from algae, since certain regions of the world are better suited than others. In the United States, the southwest and several southern states are good locations to cultivate algae. As Wogan28 observed, Texas is wellsuited for commercial algae production. The state is abundant in CO2 production, saline aquifers, and sunlight. Texas also contains many resources unique to the energy and rening industries. Borowitzka argued that geographic factors also inuence the selection of a reactor, including the cost of land and climate at the reactor site.43 For example, Betatene Ltd., which produces D. salina in Australia, uses large open ponds up to 250 ha in size. For their application, even mixing devices are unnecessary. Open ponds provide optimal growth in this case because land costs are low, seawater is free, and the climate allows production throughout the year.44 However, large open ponds have often proven unsuccessful in other regions. 3. Open Ponds The most common growth systems used for commercial purposes are open pond reactors. According to Borowitzka,44 the four most common types of commercial cultivation systems are large open ponds, circular ponds with rotating components for mixing, raceway ponds, and large bags. Open ponds are frequently designed like raceway ponds, which feature paddlewheels and bafes to promote mixing. Figures 5 and 6 illustrate examples of raceway ponds in schematic and pilot-scale forms. Optimal pond depth is a trade-off between keeping the pond shallow enough to provide sufcient light to the culture but deep enough to enhance mixing and remain unaffected by evaporation.44 Open ponds, along with most closed photobioreactors, must be connected to some form of a harvesting system, which collects the algae cells for biomass concentration, cell lysis, and oil extraction.5 From 1980 to 1996, the U.S. Department of Energy conducted a research effort within their Biofuels Program, known as the Aquatic Species Program (ASP). The ASP research focused on

Figure 6. Seambiotic pilot-scale raceway ponds. (Reprinted with kind permission from ref 59. Copyright 2008 Seambiotic.)

using open pond raceway systems to grow microalgae to produce biodiesel. The 1000 m2 ponds located in a test site in New Mexico succeeded in generating single day biomass productivities as high as 50 g/m2 d. Conclusions from this extensive study are summarized in the ASP nal report.1 Detailed economic studies of open pond reactors are not found widely in the literature but are abundant in the ASP report. The results, though outdated, provide a sense of the range of costs potentially associated with open ponds and the immense variability of price based on what the pond may be equipped with. The rst notable analysis, by Benemann et al.45 in 1978, was based on assumptions including 40 ha growth ponds with multiple channels and productivities ranging from 6-18 g/m2 d. The analysis did not consider species control, wastewater treatment, nutrients, or the utilization of algal biomass. Design aspects that were considered in the analysis included harvesting, earthworks, pumps to move and lift the water, the supply channels and piping required, transfer structures, settling ponds, and ducting for CO2. Total capital costs were estimated (in 1978 dollars) at about $9,000/ha, without contingencies or engineering. Annualized costs were estimated at about $2,000/ha based on a 15% per annum capital charge, $700/ha operating costs for labor/nutrients, and free CO2.45 Benemann et al.46 conducted another analysis in 1982 that was more thorough and featured paddle wheel mixing for the 40 ha ponds. Productivities were estimated to be twice as high, but centrifugation and solvent extraction steps were now considered. A power plant that would provide the CO2 was assumed to be only 5 km away. Several scenarios were analyzed, and total estimated capital costs ranged from $24,520 to $44,585/ ha (in 1982 dollars). Estimates of annual operating costs plus return on investment ranged from $9,830 to $20,385/ha.46 These analyses were followed up with a study by Neenan et al.47 in 1986, which included preliminary considerations of downstream processing costs and an overall price per gallon of biodiesel. Important assumptions were 30% lipid content in the algal biomass, and a 17 g/m2 d average biomass productivity. The overall projected system costs were $43,283/ha of ponds and $433/mt of algal biomass produced (in 1986 dollars).47 Finally, the ASP report discussed a fourth analysis by Weissman and Goebel48 in 1987. Due to the comprehensive nature of the analysis, the many assumptions that were used are not included here. The focus of the open pond design appeared to be to maximize productivity with little emphasis on cost reduction. The estimated capital cost was $72,000/ha

3522

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 7. Conceptual tubular reactor.

Figure 9. Conceptual FP reactor.

Figure 8. Conceptual column reactor.

(in 1987 dollars) for a system with an average productivity of 30 g/m2 d. The estimated annual cost of biomass production at the previous productivity was $273/mt.48 The previous discussion should illustrate that open pond costs can vary widely depending on the complexity of the design. Nevertheless, the ASP report concluded that all alternatives to open pond designs were cost-prohibitive at the time.1 In a 2006 review by Carvalho et al.,35 the authors also noted that recent literature did not contain many details about production costs and that these details would be necessary before reactor types could be compared effectively. Open ponds present signicant technical challenges in addition to economic challenges. A major problem with open ponds is the presence of competition and predation, as it is very difcult to maintain a monoculture of one desired strain of algae in an outdoor open environment. According to reviews by Lee and Borowitzka, the most successful commercial strains of algae grown in open ponds all thrive in extreme environments that inhibit competition. For example, Dunaliella, Spirulina, and Chlorella strains grow in environments exceptionally high in salinity, alkalinity, and nutrients, respectively.4,44 Loss of water to evaporation is yet another hindrance to the success of open ponds. However, at the heart of the problem with open ponds is the inadequate control of the design parameters necessary for optimal algae growth. 4. Closed Photobioreactors The literature often suggests that open ponds may have been overemphasized21 and that they have reached a plateau in productivity.35 Several authors articulated the need for closed systems in order to achieve future advances in large-scale algae production. They argued that as costs are reduced in the future, closed systems will become the reactors of choice for biofuel production.8,44 Numerous types of enclosed photobioreactors have been designed in an attempt to best control the growth factors discussed earlier. The three main categories most generally suitable for large-scale cultivation are tubular/horizontal, column/vertical, and at plate or at panel (FP) reactors.49 The next set of Figures 7-9 displays the three main types of closed reactors in conceptual form.

Many other designs are not suitable for large-scale production of biofuel and thus have been omitted from this discussion. Though large-scale designs are the focus, the majority of experiments comparing the designs were performed at laboratory scale. In addition, the large-scale closed system examples retrieved from the literature were often used to cultivate algae for a purpose other than biofuel production. However, the insight gained from analyzing these examples is relevant to the application of biofuel production. Some reactor designs included in literature deviate from the conventional three types of closed reactors, but these have shown limited promise. Borowitzka44 described a cylindrically shaped helical tubular design known as the BIOCOIL that was supposedly the most promising design at that time (1999). However, limited discussion of the BIOCOIL during recent years suggests that it no longer has potential. Watanabe and Hall noted that the design has radiation losses in the central area of the reactor. The authors attempted to improve it by constructing a laboratory-scale cone-shaped helical tubular reactor. This design supposedly increased the illuminated surface area while covering the same area on the ground as a regular tubular or FP reactor.50 Little has been reported on the ability of the cone-shaped design to be scaled up. Algae have also been cultivated in bag type reactors. However, according to Borowitzka, the big bag system suffers from the need to be operated indoors for adequate temperature control. If installed indoors, the large bags cannot be sufciently illuminated by articial lighting, and mixing is generally insufcient.44 The concept of closed systems resulting in higher productivities is not supported unanimously in the literature. In a review by Lee,4 the author claimed that 25 years worth of data show that volumetric productivity and cost of production are not better in closed systems compared to open ponds. However, the majority of the literature reviewed for this paper contained results contrary to that claim. 4.1. Closed Reactor Comparisons. Many key reactor comparison parameters were mentioned earlier along with design considerations. Tredici et al. asserted that photosynthetic efciency (PE) should be used in conjunction with volumetric productivity when evaluating systems operated under similar climactic conditions. The authors claimed that the PE is signicantly higher in tubular reactors compared to FP reactors because their curved surface resulted in the spatial dilution of light.7 Although some authors have claimed that FP reactors may have greater photosynthetic efciency,9 the results of Tredici et al. are convincing and it appears that PE is a drawback for FP reactors. Another drawback for FP reactors is that cell damage may occur because of the high stress resulting from aeration, a problem that has never been reported in tubular reactors. However, FP reactors have advantages over other closed reactors. In FP reactors, the oxygen path is much shorter than in tubular reactors.49 A shorter oxygen path results in FP

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3523

Table 1. Typical Advantages and Disadvantages of the Three Main Types of Closed Reactors reactor type
FP

typical advantages
shortest oxygen path low power consumption high volumetric biomass density

typical disadvantages
low photosynthetic efciency shear damage from aeration oxygen accumulation photoinhibition most land use

tubular

vertical

greatest gas exchange best exposure to light/dark cycles least land use high photosynthetic efciency

support costs scalability

Figure 10. Schematic representation of the reactors used: a bubble column (BC), an airlift reactor (ALR), and an airlift reactor with helical ow promoter (ALR+HFP).52 (Reprinted with kind permission from ref 52. Copyright 2000 John Wiley and Sons.)

reactors having lower accumulation of dissolved oxygen concentrations than horizontal reactors.24 FP reactors also consume less power than tubular reactors to achieve similar or greater mass transfer capacity.49 Power consumption is another important criterion for comparison among reactor types. Sa nchez Miro n et al.51 compared tubular and column reactors and arrived at many signicant conclusions. Tubular reactors have very limited possibility for commercial scale applications, whereas column reactors do have potential. Bubble column reactors performed better than tubular reactors because they are supposedly more suited for scale-up, require less energy for cooling because of the low surface to volume ratio, and overall outperform tubular reactors throughout the year. Under high light intensity, vertical reactors experience less photoinhibition, and under low light intensity, a vertical orientation captures more reected light.51 A vertical orientation also requires less land area.17 Molina et al. asserted that, for tubular reactors, a twolayered loop with the lower set of tubes displaced horizontally in between the upper set of tubes maximizes efciency of land use.36 Vertical reactors appear to best satisfy the design considerations outlined earlier in this paper, at least at laboratory scale. There are two main types of vertical reactors: air-lift reactors and bubble column reactors. Vertical air-lift reactors improve gas exchange, liquid ow, and exposure of cells to light.17 Airlift reactors circulate the culture without moving parts or mechanical pumping, which reduces the potential for contamination and for cell damage due to shear. The tubular photobioreactor of Molina et al., depicted earlier in Figure 4, was air-lift driven. The air-lift both circulated the uid through the loop and stripped oxygen from the culture.36 Experiments involving different types of column reactors have provided conicting results. Merchuk et al.52 compared the performance of an airlift reactor equipped with helical ow promoters (ALR + HFP) to the performance of a bubble column reactor, both at bench-scale. Figure 10 illustrates the benchscale reactors. The authors found that the ALR + HFP performed the best with regard to biomass production because improved uid dynamics led to less air and CO2 consumption, which signicantly reduced operating costs.52 In a review by Janssen et al.,9 the authors analyzed pneumatically agitated vertical column reactors, tubular reactors, and at panel reactors. The authors concluded that bubble column and air-lift reactors appear to have similar light regimes and productivity, but that bubble

column reactors perform better at higher supercial gas velocities (above 0.05 m/s) and at column heights greater than the 2.32 m. used for comparison. The authors also claimed that tubular reactors display equal or lesser photosynthetic efciency than bubble column or air-lift reactors, but that the biomass density is twice as high.9 Finally, in a review by Eriksen et al., the authors noted that airlift and bubble column reactors may be superior to stirred tank reactors because of the absence of moving mechanical components, which require greater maintenance.53 The advantages and disadvantages of different types of reactors are compared in Table 1. Table 1 reveals that each of the most common reactor types exhibit tradeoffs between key design parameters. Vertical reactors generally feature the least land use among the three closed reactor types and high photosynthetic efciency, at least on the small scales most often described in the literature. Excluding cost, these two measures of performance may be the most important when selecting a reactor conguration. However, vertical reactors are most susceptible to scalability challenges, thus making it difcult to determine the preferred reactor type among these choices for commercial scale applications. 4.2. Closed Reactor Scalability. According to Sierra et al., at panel and tubular photobioreactors have been scaled-up to sizes exceeding 1000 L, but vertical reactors are limited to an optimum size of 125 L.49 There are limited examples of largescale applications of air-lift reactors. Vunjak-Novakovic et al. described the design and operation of a pilot-scale triangular air-lift unit fed by ue gas. The pilot-scale unit was composed of 30 ALRs, each containing a volume of 30 L. The system was installed and tested under actual conditions on the roof of the Cogeneration Power Plant at the Massachusetts Institute of Technology.54 Figure 11 contains images of the triangular airlift reactor conguration: Tubular reactors can be scaled-up by either increasing the length or diameter of the tubes. Either route presents technical challenges. An increase in tube length results in unacceptable concentrations of dissolved oxygen along the tubes. In contrast, increasing the tube diameter may be more promising as long as the entire culture can be illuminated sufciently. However, one of the major problems of increasing the diameter is light stratication.23,36 Molina et al. noted that scale-up of the airlift driven tubular reactor discussed earlier would be challenging.36 However, Chisti was optimistic about the scale-up of tubular reactors and claimed that only tubular photobioreactors and raceway ponds are suitable for large-scale production.5 Janssen et al. concluded that scale-up of closed systems is only possible by increasing the number of small units in a production scheme. This method becomes extremely expensive, since each unit requires a variety of devices that control the wide range of growth factors discussed earlier in this paper. In

3524

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

Figure 11. Inclined-tube ALR conguration: (A) schematic presentation of one airlift triangle. Solid arrows indicate the direction of the gas ow, and open arrows indicate the direction of the liquid ow (B) An array of 30 ALRs, each with a volume of 30 L, with an algal culture grown on a ue gas. Inset: installation of the array of ALRs on the roof of the MIT Cogeneration Power Plant.54 (Reprinted with kind permission from ref 54. Copyright 2005 American Chemical Society.)

Figure 12. Commercial-scale photobioreactor facility in Klotze, Germany. (Reprinted with kind permission from ref 3. Copyright 2006 Society of Fermentation and Bioengineering.)

addition, maintaining a monoculture in all of the units becomes challenging as the number of units to monitor and service grows.9 Commercial-scale closed photobioreactors have not been widely reported in scientic literature. Closed systems for commercial applications began in Japan, Israel, and Germany.3 Janssen et al. claimed to describe the worlds largest example of a closed reactor system as of the year 2003. The 700 m3 tubular production system in Klotze, Germany, consisted of 20 separate 35 m3 units. Chlorella Vulgaris was mechanically pumped through horizontal glass tubes with 4 cm diameter and 25 000 m of length for each unit. The authors questioned the estimated productivity of 150 tons of biomass per year, and no other gures were reported in the review.9 A review by Spolaore et al.3 also mentioned the Klotze facility and states a production rate of 130-150 tons dry biomass/y. Figure 12 is an image of the Klotze facility. The review by Janssen et al. also claimed to describe the largest at panel reactor example, which was studied by Richmond and Cheng-Wu.55 The large-scale reactor described was composed of individual units of 200 L, and the units were connected as illustrated in Figure 13. 4.3. Closed Reactor Economics. The paramount advantages of closed systems are the greater control of design parameters and the growth of algae essentially as a monoculture. However, economics are currently a major drawback for closed systems.

Between 2002 and 2004, $100/m2 was an estimate of photobioreactor capital costs used in the literature, with the expectation of signicant cost reductions as technology improved.56 In a review by Schenk et al., the authors claimed that reactor costs should not exceed $15/m2 based on energy costs and productivities from 2008. The estimated setup costs for closed reactors were generally ten times higher than for open ponds.8 In a review by Chisti,5 direct comparisons were made between the production costs of hypothetical facilities producing 100 000 kg of biomass annually using either photobioreactors or raceway ponds. Chisti found that the estimated production costs were $2.95 and $3.80/kg of biomass for closed reactors and raceway ponds, respectively. Under a scaled-up scenario of 10 000 tons of biomass produced per year, the estimated production costs were $0.47 and $0.60/kg of biomass for closed versus open reactors.5 Note that this analysis did not consider the capital costs involved with creating either facility, but it did show that production costs are expected to be lower in closed systems. Because of economic considerations, many authors have concluded that closed reactors can only be used for the production of high-value products.12,35 The ASP report contained an important conclusion regarding the evaluation of the potential economics of algae production, whether it involved open or closed systems. The report asserts that high value byproducts or coproducts, such as pigments, vitamins, or specialty chemicals created from the remaining biomass, should be excluded from the cost analysis. These products would be produced in such large amounts that they would saturate potential markets. An exception would be large byproduct markets such as for animal feeds, and indeed, the authors believed that a likely route for commercial scale production will utilize specialty foods and animal feeds coproduction.1 However, Chisti argued that most of the biomass remaining after oil extraction should be made into biogas using anaerobic digestion. The resulting biogas would then be used to meet the energy needs of growing and processing algae in the same facility. Economic benets from using this approach include the sale of surplus energy, nutrient-rich fertilizer, and irrigation water all produced while making biogas.41 5. Combinations of Open and Closed Systems Some authors believe that combining open and closed reactors is the most effective conguration for growing algae.8 Huntley

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

3525

Figure 13. A schematic drawing of 2 units, 200 L each, connected together. (a) point of connection of two reactor units, (b) inner supports, (c) braces for keeping together the front and back plates, (d) distance between the bottom of the reactor and the inner supports, (e) passage made between the two units to create a common volume between units.55 (Reprinted with kind permission from ref 55. Copyright 2001 Elsevier.)

and Redalje,56 as well as Olaizola,57 described a two-stage commercial-scale production system that was in continuous operation from December 1997 to September 2001. The Aquasearch facility, located in Hawaii, was designed to maximize the production of astaxanthin from Haematococcus pluVialis, but the strain also produces oil under the same conditions. The facility featured 25 000 L closed photobioreactors and 50 000 L open ponds, with a total capacity of over 600 000 L equally divided between photobioreactors and ponds. During the nal year of operation, the average areal productivity was 10.2 g/m2 d, which corresponded to a photosynthetic efciency of 3.0%.56 The two-stage process began with growth in an industrialscale closed reactor. The highly controlled environment in this step maximized cell growth. Next, the algae were exposed to nutrient deprivation by being transferred to an open pond reactor. Finally, the stress increased the lipid content of each cell. An important guideline to adhere to when considering a hybrid reactor scheme is minimizing the residence time of the algae in the open pond, where they are vulnerable to contamination.56 Rodol et al. also considered a similar two stage process, in which 22% of the hypothetical plant is dedicated to biomass production under N-sufciency and the remainder is devoted to oil production under N-deprivation.38 Similar to the reactor congurations discussed earlier, critical drawbacks are present with the two-stage approach. The capital and operating costs for both a commercial-scale closed reactor and a commercial-scale open pond are likely to be signicantly higher than for one reactor. In a review by Vasudevan and Briggs, it was observed that because the facility described by Huntley and Redalje produced astaxanthin, which is a highvalue product, the economics were signicantly better than the economics based on primarily biofuel production.58 In addition, the land requirements are much greater than for one reactor and the increased land use reduces the productivity per area. 6. Conclusion The cultivation of microalgae for biofuel production requires high levels of biomass productivity per area and minimal costs. Major technical and economic challenges impede the selection of an optimal reactor type at the commercial scale. Without detailed economic considerations, closed reactors appear to perform better than open ponds because they maintain favorable growth conditions and are less vulnerable to contamination. The

best reactor type, based on photosynthetic efciency and areal productivity, appears to be column reactors, at least on the small scale used in experiments from the literature. However, technical constraints prevent the size of this reactor type from being increased to commercial scale without the use of multiple small units, which are unlikely to be economical. Combinations of open and closed reactors seem promising from a productivity perspective. However, there is not enough economic information available to assess whether the increased productivity can offset the extra capital investment required, particularly with regard to biofuel applications. Thus, at this time, no specic reactor type is optimal for the commercial cultivation of microalgae for biofuel production. This agrees with the general conclusion arrived at by other authors.12,35 Literature Cited
(1) Sheehan, J.; Dunahay, T.; Benemann, J.; Roessler, P. A Look Back at the U.S. Department of Energys Aquatic Species Program: Biodiesel from Algae; U.S. Department of Energy, 1998. doi: 10.2172/15003040. (2) Demirbas, A. Importance of biodiesel as transportation fuel. Energy Policy 2007, 35 (9), 46614670. (3) Spolaore, P.; Joannis-Cassan, C.; Duran, E.; Isambert, A. Commercial applications of microalgae. J. Biosci. Bioeng. 2006, 101 (2), 8796. (4) Lee, Y. K. Microalgal mass culture systems and methods: Their limitation and potential. J. Appl. Phycol. 2001, 13 (4), 307315. (5) Chisti, Y. Biodiesel from microalgae. Biotechnol. AdV. 2007, 25 (3), 294306. (6) Mussgnug, J. H.; Thomas-Hall, S.; Rupprecht, J.; Foo, A.; Klassen, V.; McDowall, A.; Schenk, P. M.; Kruse, O.; Hankamer, B. Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol. J. 2007, 5 (6), 802814. (7) Tredici, M. R.; Zittelli, G. C. Efciency of sunlight utilization: Tubular versus at photobioreactors. Biotechnol. Bioeng. 1998, 57 (2), 187 197. (8) Schenk, P. M.; Thomas-Hall, S. R.; Stephens, E.; Marx, U. C.; Mussgnug, J. H.; Posten, C.; Kruse, O.; Hankamer, B. Second generation biofuels: High-efciency microalgae for biodiesel production. Bioenergy Res. 2008, 1 (1), 19391234. (9) Janssen, M.; Tramper, J.; Mur, L. R.; Wijffels, R. H. Enclosed outdoor photobioreactors: Light regime, photosynthetic efciency, scaleup, and future prospects. Biotechnol. Bioeng. 2003, 81 (2), 193210. (10) Richmond, A. Principles for attaining maximal microalgal productivity in photobioreactors: an overview. Hydrobiologia 2004, 512 (1-3), 3337. (11) Park, K.-H.; Lee, C.-G. Effectiveness of ashing light for increasing photosynthetic efciency of microalgal cultures over a critical cell density. Biotechnol. Bioprocess Eng. 2001, 6, 189193. (12) Pulz, O.; Scheibenbogen, K. Photobioreactors: Design and performance with respect to light energy input. AdV. Biochem. Eng./Biotechnol. 1998, 59, 123152.

3526

Ind. Eng. Chem. Res., Vol. 49, No. 8, 2010

(37) Mandalam, R. K.; Palsson, B. O. Elemental balancing of biomass and medium composition enhances growth capacity in high-density Chlorella vulgaris cultures. Biotechnol. Bioeng. 1998, 59 (5), 605611. (38) Rodol, L.; Zittelli, G. C.; Bassi, N.; Padovani, G.; Biondi, N.; Bonini, G.; Tredici, M. R. Microalgae for Oil: Strain Selection, Induction of Lipid Synthesis and Outdoor Mass Cultivation in a Low-Cost Photobioreactor. Biotechnol. Bioeng. 2009, 102 (1), 100112. (39) Coleman, J. R.; Colman, B. Inorganic carbon accumulation and photosynthesis in a blue-green alga as a function of external pH. J. Phycol 1981, (27), 28. (40) Lee, Y. K.; Pirt, S. J. CO2 absorption rate in an algal culture: Effect of pH. Plant. Physiol. 1984, (67), 917921. (41) Chisti, Y. Biodiesel from microalgae beats bioethanol. Trends Biotechnol. 2008, 26 (3), 126131. (42) Pulz, O.; Gross, W. Valuable products from biotechnology of microalgae. Appl. Microbiol. Biotechnol. 2004, 65 (6), 635648. (43) Borowitzka, M. A. Algal biotechnology products and processes: matching science and economics. J. Appl. Phycol. 1992, 4 (3), 267279. (44) Borowitzka, M. A. Commercial production of microalgae: ponds, tanks, tubes and fermenters. J. Biotechnol. 1999, 70 (1-3), 313321. (45) Benemann, J. R. P., P.; Oswald, W. J. Cost analysis of microalgae biomass systems; HCP/t1-605-01 Under Contract EX-78-X-01-1 605; Final Report prepared for the U.S. Dept. of Energy, 1978. (46) Benemann, J. R. A., D.C.; Weissman, J. C. Microalgae as a source of liquid fuels, appendix: technical feasibility analysis; Final Report, U.S. Department of Energy: Washington, D. C., 1982; p 126. (47) Neenan, B. F., D.; Hill, A.; McIntosh, R.; Terry, K. Fuels from microalgae: Technology status, potential, and research requirements; SERI/ SP-231-2550; Report, Solar Energy Research Institute: Golden, CO: 1986; p 158. (48) Weissman, J. C. ; Goebel, R. P. Design and analysis of pond systems for the purpose of producing fuels; SERI/STR-231-2840; Report, Solar Energy Research Institute: Golden, CO: 1987. (49) Sierra, E.; Acien, F. G.; Fernandez, J. M.; Garcia, J. L.; Gonzalez, C.; Molina, E. Characterization of a at plate photobioreactor for the production of microalgae. Chem. Eng. J. 2008, 138 (1-3), 136147. (50) Watanabe, Y.; Hall, D. O. Photosynthetic production of the lamentous cyanobacterium Spirulina platensis in a cone shaped helical tubular photobioreactor. Appl. Microbiol. Biotechnol. 1996, 44 (6), 693 698. (51) Sa nchez Miro n, A.; Contreras Go mez, A.; Garc a Camacho, F.; Molina Grima, E.; Chisti, Y. Comparative evaluation of compact photobioreactors for large-scale monoculture of microalgae. J. Biotechnol. Biotechnol. Aspects Marine Sponges 1999, 70 (1-3), 249270. (52) Merchuk, J C.; Mukmenev, M. G., I. Comparison of photobioreactors for cultivation of the red microalga Porphyridium sp. J. Chem. Technol. Biotechnol. 2000, 75 (12), 11191126. (53) Eriksen, N. T. The technology of microalgal culturing. Biotechnol. Lett. 2008, 30 (9), 15251536. (54) Vunjak-Novakovic, G.; Kim, Y.; Wu, X. X.; Berzin, I.; Merchuk, J. C. Air-lift bioreactors for algal growth on ue gas: Mathematical modeling and pilot-plant studies. Ind. Eng. Chem. Res. 2005, 44 (16), 61546163. (55) Richmond, A.; Cheng-Wu, Z. Optimization of a at plate glass reactor for mass production of Nannochloropsis sp outdoors. J. Biotechnol. 2001, 85 (3), 259269. (56) Huntley, M. E.; Redalje, D. G. CO2 mitigation and renewable oil from photosynthetic microbes: A new appraisal. Mitigation Adapt. Strat. Global Change 2007, 12 (4), 573608. (57) Olaizola, M. Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J. Appl. Phycol. 2000, 12 (3-5), 499506. (58) Vasudevan, P. T.; Briggs, M. Biodiesel production-current state of the art and challenges. J. Ind. Microbiol. Biotechnol. 2008, 35 (5), 421 430. (59) Seambiotic. http://www.seambiotic.com (accessed July 6, 2009).

(13) Goldman, J. C. Outdoor Algal Mass-Cultures 0.2. Photosynthetic Yield Limitations. Water Res. 1979, 13 (2), 119136. (14) Matthijs, H. C. P.; Balke, H.; VanHes, U. M.; Kroon, B. M. A.; Mur, L. R.; Binot, R. A. Application of light-emitting diodes in bioreactors: Flashing light effects and energy economy in algal culture (Chlorella pyrenoidosa). Biotechnol. Bioeng. 1996, 50 (1), 98107. (15) Janssen, M.; Slenders, P.; Tramper, J.; Mur, L. R.; Wijffels, R. H. Photosynthetic efciency of Dunaliella tertiolecta under short light/dark cycles. Enzyme Microbial. Technol. 2001, 29 (4-5), 298305. (16) Gordon, J. M.; Polle, J. E. W. Ultrahigh bioproductivity from algae. Appl. Microbiol. Biotechnol. 2007, 76 (5), 969975. (17) Camacho, F. G.; Gomez, A. C.; Fernandez, F. G. A.; Sevilla, J. F.; Grima, E. M. Use of concentric-tube airlift photobioreactors for microalgal outdoor mass cultures. Enzyme Microbial. Technol. 1999, 24 (3-4), 164 172. (18) Zu, N.; Richmond, A. Light-path length and population density in photoacclimation of Nannochloropsis sp. (Eustigmatophyceae). J. Appl. Phycol. 2000, 12 (3-5), 349354. (19) Feuermann, D.; Gordon, J. M.; Huleihil, M. Solar ber-optic minidisit-concentrators: First experimental results and eld experience. Solar Energy 2002, 72 (6), 459472. (20) Zijffers, J. W. F.; Janssen, M.; Tramper, J.; Wijffels, R. H. Design process of an area-efcient photobioreactor. Marine Biotechnol. 2008, 10 (4), 404415. (21) Suh, I. S.; Lee, C. G. Photobioreactor engineering: Design and performance. Biotechnol. Bioprocess Eng. 2003, 8 (6), 313321. (22) Qiang, H.; Richmond, A. Productivity and photosynthetic efciency of Spirulina platensis as affected by light intensity, algal density and rate of mixing in a at plate photobioreactor. J. Appl. Phycol. 1996, 8 (2), 139 145. (23) Ugwu, C. U.; Ogbonna, J. C.; Tanaka, H. Characterization of light utilization and biomass yields of Chlorella sorokiniana in inclined outdoor tubular photobioreactors equipped with static mixers. Process Biochem. 2005, 40 (11), 34063411. (24) Ugwu, C. U.; Aoyagi, H.; Uchiyama, H. Photobioreactors for mass cultivation of algae. Bioresour. Technol. 2008, 99 (10), 40214028. (25) Eriksen, N. T.; Poulsen, B. R.; Iversen, J. J. L. Dual sparging laboratory-scale photobioreactor for continuous production of microalgae. J. Appl. Phycol. 1998, 10 (4), 377382. (26) Barbosa, M. J.; Hadiyanto; Wijffels, R. H. Overcoming shear stress of microalgae cultures in sparged photobioreactors. Biotechnol. Bioeng. 2004, 85 (1), 7885. (27) Berndes, G. Bioenergy and water--the implications of large-scale bioenergy production for water use and supply. Global EnViron. Change 2002, 12 (4), 253271. (28) Wogan, D. M.; Silva, A. K. D.; Webber, M. E.; Stautberg, E. Algae: Pond Powered Biofuels; ATI CleanEnergy Incubator, The University of Texas at Austin: Austin, November 19 , 2008; pp 1-23. (29) Yun, Y.-S.; Lee, S. B.; Park, J. M.; Lee, C.-I.; Yang, J.-W. Carbon Dioxide Fixation by Algal Cultivation Using Wastewater Nutrients. J. Chem. Technol. Biotechnol. 1997, 69 (4), 451455. (30) Rao, A. R.; Dayananda, C.; Sarada, R.; Shamala, T. R.; Ravishankar, G. A. Effect of salinity on growth of green alga Botryococcus braunii and its constituents. Bioresour. Technol. 2007, 98 (3), 560564. (31) Abu-Rezq, T. S.; Al-Musallam, L.; Al-Shimmari, J.; Dias, P. Optimum production conditions for different high-quality marine algae. Hydrobiologia 1999, 403, 97107. (32) Aslan, Sebnem; Kapdan, I. K. Batch kinetics of nitrogen and phosphorus removal from synthetic wastewater by algae. Ecol. Eng. 2006, 28 (1), 6470. (33) Lee, Y.-K.; Tay, H.-S. High CO2 partial pressure depresses productivity and bioenergetic growth yield of Chlorella pyrenoidosa culture. J. Appl. Phycol. 1991, 3, 95101. (34) Doucha, J.; Straka, F.; Livansky, K. Utilization of ue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin-layer photobioreactor. J. Appl. Phycol. 2005, 17 (5), 403412. (35) Carvalho, A. P.; Meireles, L. A.; Malcata, F. X. Microalgal reactors: A review of enclosed system designs and performances. Biotechnol. Prog. 2006, 22 (6), 14901506. (36) Molina, E.; Fernandez, J.; Acien, F. G.; Chisti, Y. Tubular photobioreactor design for algal cultures. J. Biotechnol. 2001, 92 (2), 113 131.

ReceiVed for reView September 16, 2009 ReVised manuscript receiVed February 26, 2010 Accepted March 1, 2010 IE901459U