Abstract
The world is facing energy crisis and environmental issues due to the depletion of fossil fuels and increasing CO2 concentration in the atmosphere. Growing microalgae can contribute to practical solutions for these global problems because they can harvest solar energy and capture CO2 by converting it into biofuel using photosynthesis. Microalgae are robust organisms capable of rapid growth under a variety of conditions including in open ponds or closed photobioreactors. Their reduced biomass compounds can be used as the feedstock for mass production of a variety of biofuels. As another advantage, their ability to accumulate or secrete biofuels can be controlled by changing their growth conditions or metabolic engineering. This review is aimed to highlight different forms of biofuels produced by microalgae and the approaches taken to improve their biofuel productivity. The costs for industrial-scale production of algal biofuels in open ponds or closed photobioreactors are analyzed. Different strategies for photoproduction of hydrogen by the hydrogenase enzyme of green algae are discussed. Algae are also good sources of biodiesel since some species can make large quantities of lipids as their biomass. The lipid contents for some of the best oil-producing strains of algae in optimized growth conditions are reviewed. The potential of microalgae for producing petroleum related chemicals or ready-make fuels such as bioethanol, triterpenic hydrocarbons, isobutyraldehyde, isobutanol, and isoprene from their biomass are also presented.
Similar content being viewed by others
Abbreviations
- Chl:
-
Chlorophyll
- DMAPP:
-
Dimethylallyl diphosphate
- FAMEs:
-
Fatty acid methyl esters
- FDX:
-
Ferredoxin
- FFA:
-
Free fatty acid
- FNR:
-
Ferredoxin-NADP+ reductase enzyme
- G3P:
-
Glyceraldehyde-3-phosphate
- IPP:
-
Isopentenyl diphosphate
- LHC:
-
Light-harvesting complex
- MEP:
-
Methyl-erythritol-4-phosphate
- P:
-
Primary electron donor
- PSI:
-
Photosystem I
- PSII:
-
Photosystem II
- QA :
-
Tightly-bound plastoquinone
- QB :
-
Mobile plastoquinone
- RuBisCO:
-
Ribulose bis-phosphate carboxylase-oxygenase
- TAG:
-
Triacylglycerols
References
Adams C, Godfrey V, Wahlen B, Seefeldt L, Bugbee B (2013) Understanding precision nitrogen stress to optimize the growth and lipid content tradeoff in oleaginous green microalgae. Bioresour Technol 131:188–194
Ahn JW, Hwangbo K, Lee SY, Choi HG, Park YI, Liu JR, Jeong WJ (2012) A new Arctic Chlorella species for biodiesel production. Bioresour Technol 125:340–343
Araujo GS, Matos LJBL, Goncalves LRB, Fernandes FAN, Farias WRL (2011) Bioprospecting for oil producing microalgal strains: evaluation of oil and biomass production for ten microalgal strains. Bioresour Technol 102(8):5248–5250
Arudchelvam Y, Nirmalakhandan N (2012) Optimizing net energy gain in algal cultivation for biodiesel production. Bioresour Technol 114:294–302
Atsumi S, Higashide W, Liao JC (2009) Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat Biotechnol 27(12):1177–1180
Barber J, Archer MD (2001) P680, the primary electron donor of photosystem II. J Photochem Photobiol A 142:97–106
Barbosa MJ, Zijffers JW, Nisworo A, Vaes W, van Schoonhoven J, Wijffels RH (2005) Optimization of biomass, vitamins, and carotenoid yield on light energy in a flat-panel reactor using the A-stat technique. Biotechnol Bioeng 89(2):233–242
Ben-Shem A, Frolow F, Nelson N (2003) Crystal structure of plant photosystem I. Nature 426:630–635
Blankenship RE, Govindjee (2007) Photosynthesis. The encyclopedia of science and technology, 10th edn. McGraw Hill Publishers, New York, pp 468–475
Bolton JR, Hall DO (1991) The maximum efficiency of photosynthesis. Photochem Photobiol 53(4):545–548
Breuer G, Lamers PP, Martens DE, Draaisma RB, Wijffels RH (2012) The impact of nitrogen starvation on the dynamics of triacylglycerol accumulation in nine microalgae strains. Bioresour Technol 124:217–226
Carrieri D, Wawrousek K, Eckert C, Yu JP, Maness PC (2011) The role of the bidirectional hydrogenase in cyanobacteria. Bioresour Technol 102(18):8368–8377
Chandran SS, Kealey JT, Reeves CD (2011) Microbial production of isoprenoids. Process Biochem 46(9):1703–1710
Chen HC, Newton AJ, Melis A (2005) Role of SulP, a nuclear-encoded chloroplast sulfate permease, in sulfate transport and H-2 evolution in Chlamydomonas reinhardtii. Photosynth Res 84(1–3):289–296
Chisti Y (2008) Biodiesel from microalgae beats bioethanol. Trends Biotechnol 26(3):126–131
Chiu SY, Kao CY, Chen CH, Kuan TC, Ong SC, Lin CS (2008) Reduction of CO2 by a high-density culture of Chlorella sp. in a semicontinuous photobioreactor. Bioresour Technol 99(9):3389–3396
Choi SP, Nguyen MT, Sim SJ (2010) Enzymatic pretreatment of Chlamydomonas reinhardtii biomass for ethanol production. Bioresour Technol 101(14):5330–5336
Deng MD, Coleman JR (1999) Ethanol synthesis by genetic engineering in cyanobacteria. Appl Environ Microbiol 65(2):523–528
Eriksen NT (2008) The technology of microalgal culturing. Biotechnol Lett 30(9):1525–1536
Eriksen NT, Geest T, Iversen JJL (1996) Phototrophic growth in the lumostat: a photo-bioreactor with on-line optimization of light intensity. J Appl Phycol 8(4–5):345–352
Eriksen NT, Poulsen BR, Iversen JJL (1998) Dual sparging laboratory-scale photobioreactor for continuous production of microalgae. J Appl Phycol 10(4):377–382
Eroglu E, Melis A (2010) Extracellular terpenoid hydrocarbon extraction and quantitation from the green microalgae Botryococcus braunii var. Showa. Bioresour Technol 101(7):2359–2366
Eroglu E, Melis A (2011) Photobiological hydrogen production: recent advances and state of the art. Bioresour Technol 102(18):8403–8413
Florin L, Tsokoglou A, Happe T (2001) A novel type of iron hydrogenase in the green alga Scenedesmus obliquus is linked to the photosynthetic electron transport chain. J Biol Chem 276(9):6125–6132
Flynn T, Ghirardi ML, Seibert M (2002) Accumulation of O2-tolerant phenotypes in H2-producing strains of Chlamydomonas reinhardtii by sequential applications of chemical mutagenesis and selection. Int J Hydrogen Energy 27(11–12):1421–1430
Frenz J, Largeau C, Casadevall E, Kollerup F, Daugulis AJ (1989) Hydrocarbon recovery and biocompatibility of solvents for extraction from cultures of Botryococcus braunii. Biotechnol Bioeng 34(6):755–762
Gallagher BJ (2011) The economics of producing biodiesel from algae. Renew Energy 36(1):158–162
Ghirardi ML, Zhang JP, Lee JW, Flynn T, Seibert M, Greenbaum E, Melis A (2000) Microalgae: a green source of renewable H2. Trends Biotechnol 18(12):506–511
Ghirardi ML, King PW, Posewitz MC, Maness PC, Fedorov A, Kim K, Cohen J, Schulten K, Seibert M (2005) Approaches to developing biological H2-photoproducing organisms and processes. Biochem Soc Trans 33:70–72
Giakoumis EG (2013) A statistical investigation of biodiesel physical and chemical properties, and their correlation with the degree of unsaturation. Renew Energy 50:858–878
Gimmler H, Degenhard B (2001) Alkaliphilic and alkali-tolerant algae. In: Rai LC, Gaur JP (eds) Algal adaptation to environmental stresses: physiological, biochemical, and molecular mechanisms. Springer, Berlin, pp 291–321
Girbal L, von Abendroth G, Winkler M, Benton PM, Meynial-Salles I, Croux C, Peters JW, Happe T, Soucaille P (2005) Homologous and heterologous overexpression in Clostridium acetobutylicum and characterization of purified clostridial and algal Fe-only hydrogenases with high specific activities. Appl Environ Microbiol 71(5):2777–2781
Glick RE, Melis A (1988) Minimum photosynthetic unit size in system-I and system-II of barley chloroplasts. Biochim Biophys Acta 934(1):151–155
Greenbaum E (1982) Photosynthetic hydrogen and oxygen production—kinetic-studies. Science 215(4530):291–293
Groot ML, Pawlowicz NP, van Wilderen LJGW, Breton J, van Stokkum IHM, van Grondelle R (2005) Initial electron donor and acceptor in isolated photosystem II reaction centers identified with femtosecond mid-IR spectroscopy. Proc Natl Acad Sci USA 102(37):13087–13092
Gross W (2000) Ecophysiology of algae living in highly acidic environments. Hydrobiologia 433(1–3):31–37
Hama S, Kondo A (2012) Enzymatic biodiesel production: an overview of potential feedstocks and process development. Bioresour Technol (in press)
Harun R, Danquah MK (2011) Influence of acid pre-treatment on microalgal biomass for bioethanol production. Process Biochem 46(1):304–309
Hemschemeier A, Fouchard S, Cournac L, Peltier G, Happe T (2008) Hydrogen production by Chlamydomonas reinhardtii: an elaborate interplay of electron sources and sinks. Planta 227(2):397–407
Hillen LW, Pollard G, Wake LV, White N (1982) Hydrocracking of the oils of Botryococcus braunii to transport fuels. Biotechnol Bioeng 24(1):193–205
Ho SH, Huang SW, Chen CY, Hasunuma T, Kondo A, Chang JS (2012) Bioethanol production using carbohydrate-rich microalgae biomass as feedstock. Bioresour Technol (in press)
Holzwarth AR, Muller MG, Reus M, Nowaczyk M, Sander J, Rogner M (2006) Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: pheophytin is the primary electron acceptor. Proc Natl Acad Sci USA 103(18):6895–6900
Hoshino T, Johnson DJ, Cuello JL (2012) Design of new strategy for green algal photo-hydrogen production: spectral-selective photosystem I activation and photosystem II deactivation. Bioresour Technol 120:233–240
Johnson MB, Wen ZY (2009) Production of biodiesel fuel from the Microalga Schizochytrium limacinum by direct transesterification of algal biomass. Energy Fuels 23:5179–5183
Joliot P, Barbieri G, Chabaud R (1969) Un nouveau modele des centers photochimiques du systeme II. Photochem Photobiol 10:309–329
Karmakar A, Karmakar S, Mukherjee S (2010) Properties of various plants and animals feedstocks for biodiesel production. Bioresour Technol 101(19):7201–7210
Kiang NY, Siefert J, Govindjee, Blankenship RE (2007) Spectral signatures of photosynthesis I. Review of Earth organisms. Astrobiology 7(1):222–251
Kim JP, Kim KR, Choi SP, Han SJ, Kim MS, Sim SJ (2010) Repeated production of hydrogen by sulfate re-addition in sulfur deprived culture of Chlamydomonas reinhardtii. Int J Hydrogen Energy 35(24):13387–13391
Kok B (1957) Absorption changes induced by the photochemical reaction of photosynthesis. Nature 179:583–584
Kok B, Forbush B, McGolin M (1970) Cooperation of charges in photosynthetic O2 evolution-I. A linear four step mechanism. Photochem Photobiol 11:457–475
Kondo T, Arakawa M, Wakayama T, Miyake J (2002) Hydrogen production by combining two types of photosynthetic bacteria with different characteristics. Int J Hydrogen Energy 27(11–12):1303–1308
Kumar K, Dasgupta CN, Nayak B, Lindblad P, Das D (2011) Development of suitable photobioreactors for CO2 sequestration addressing global warming using green algae and cyanobacteria. Bioresour Technol 102(8):4945–4953
Lai JQ, Hu ZL, Wang PW, Yang Z (2012) Enzymatic production of microalgal biodiesel in ionic liquid [BMIm][PF6]. Fuel 95(1):329–333
Lee YK (1997) Commercial production of microalgae in the Asia-Pacific rim. J Appl Phycol 9(5):403–411
Lee DH (2011) Algal biodiesel economy and competition among bio-fuels. Bioresour Technol 102(1):43–49
Li X, Xu H, Wu Q (2007) Large-scale biodiesel production from microalga Chlorella protothecoides through heterotrophic cultivation in bioreactors. Biotechnol Bioeng 98(4):764–771
Lindberg P, Park S, Melis A (2010) Engineering a platform for photosynthetic isoprene production in cyanobacteria, using Synechocystis as the model organism. Metab Eng 12(1):70–79
Loll B, Kern J, Saenger W, Zouni A, Biesiadka J (2005) Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II. Nature 438:1040–1044
Lopez MC, Sanchez Edel R, Lopez JL, Fernandez FG, Sevilla JM, Rivas J, Guerrero MG, Grima EM (2006) Comparative analysis of the outdoor culture of Haematococcus pluvialis in tubular and bubble column photobioreactors. J Biotechnol 123(3):329–342
Lv JM, Cheng LH, Xu XH, Zhang L, Chen HL (2010) Enhanced lipid production of Chlorella vulgaris by adjustment of cultivation conditions. Bioresour Technol 101(17):6797–6804
Matsunaga T, Takeyama H, Sudo H, Oyama N, Ariura S, Takano H, Hirano M, Burgess JG, Sode K, Nakamura N (1991) Glutamate production from CO2 by marine cyanobacterium Synechococcus sp. using a novel biosolar reactor employing light-diffusing optical fibers. Appl Biochem Biotechnol 28–9:157–167
Matsushika A, Sawayama S (2011) Comparative study on a series of recombinant flocculent Saccharomyces cerevisiae strains with different expression levels of xylose reductase and xylulokinase. Enzyme Microb Technol 48(6–7):466–471
McKinlay JB, Harwood CS (2010) Photobiological production of hydrogen gas as a biofuel. Curr Opin Biotechnol 21(3):244–251
Melis A (2002) Green alga hydrogen production: progress, challenges and prospects. Int J Hydrogen Energy 27(11–12):1217–1228
Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antennae to maximize efficiency. Plant Sci 177(4):272–280
Melis A, Melnicki MR (2006) Integrated biological hydrogen production. Int J Hydrogen Energy 31(11):1563–1573
Melis A, Zhang LP, Forestier M, Ghirardi ML, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122(1):127–135
Merchant SS, Kropat J, Liu BS, Shaw J, Warakanont J (2012) TAG, You’re it! Chlamydomonas as a reference organism for understanding algal triacylglycerol accumulation. Curr Opin Biotechnol 23(3):352–363
Metzger P, Largeau C (2005) Botryococcus braunii: a rich source for hydrocarbons and related ether lipids. Appl Microbiol Biotechnol 66(5):486–496
Miranda JR, Passarinho PC, Gouveia L (2012) Pre-treatment optimization of Scenedesmus obliquus microalga for bioethanol production. Bioresour Technol 104:342–348
Mulder DW, Boyd ES, Sarma R, Lange RK, Endrizzi JA, Broderick JB, Peters JW (2010) Stepwise [FeFe]-hydrogenase H-cluster assembly revealed in the structure of HydA(Delta EFG). Nature 465(7295):248–251
Murata N, Takahashi S, Nishiyama Y, Allakhverdiev SI (2007) Photoinhibition of photosystem II under environmental stress. Biochim Biophys Acta 1767(6):414–421
Mussgnug JH, Thomas-Hall S, Rupprecht J, Foo A, Klassen V, McDowall A, Schenk PM, Kruse O, Hankamer B (2007) Engineering photosynthetic light capture: impacts on improved solar energy to biomass conversion. Plant Biotechnol J 5(6):802–814
Niehaus TD, Okada S, Devarenne TP, Watt DS, Sviripa V, Chappell J (2011) Identification of unique mechanisms for triterpene biosynthesis in Botryococcus braunii. Proc Natl Acad Sci USA 108(30):12260–12265
OECD/FAO. 2012. OECD-FAO agricultural outlook 2012–2021. Paris: OECD Publishing and FAO. http://dx.doi.org/10.1787/agr_outlook-2012-en. Accessed 3 April 2013
Olaizola M (2000) Commercial production of astaxanthin from Haematococcus pluvialis using 25,000-liter outdoor photobioreactors. J Appl Phycol 12(3–5):499–506
Oren A (2010) Acidophiles. Encyclopedia of life sciences. Macmillian Press, London, pp 1–14
Pienkos PT, Darzins A (2009) The promise and challenges of microalgal-derived biofuels. Biofuels Bioprod Biorefining 3(4):431–440
Polle JEW, Melis A (1999) Recovery of the photosynthetic apparatus from photoinhibition during dark incubation of the green alga Dunaliella salina. Aust J Plant Physiol 26(7):679–686
Pulz O (2001) Photobioreactors: production systems for phototrophic microorganisms. Appl Microbiol Biotechnol 57(3):287–293
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65(6):635–648
Quinn JC, Catton K, Wagner N, Bradley TH (2012a) Current large-scale US biofuel potential from microalgae cultivated in photobioreactors. Bioenergy Res 5(1):49–60
Quinn JC, Yates T, Douglas N, Weyer K, Butler J, Bradley TH, Lammers PJ (2012b) Nannochloropsis production metrics in a scalable outdoor photobioreactor for commercial applications. Bioresour Technol 117:164–171
Rabinowitch EI, Govindjee (1965) The role of chlorophyll in photosynthesis. Sci Am 213:74–83
Raszewski G, Diner BA, Schlodder E, Renger T (2008) Spectroscopic properties of reaction center pigments in photosystem II core complexes: revision of the multimer model. Biophys J 95(1):105–119
Rodolfi L, Zittelli GC, Bassi N, Padovani G, Biondi N, Bonini G, Tredici MR (2009) Microalgae for oil: strain selection, induction of lipid synthesis and photobioreactor. Biotechnol Bioeng 102(1):100–112
Samori C, Torri C, Samori G, Fabbri D, Galletti P, Guerrini F, Pistocchi R, Tagliavini E (2010) Extraction of hydrocarbons from microalga Botryococcus braunii with switchable solvents. Bioresour Technol 101(9):3274–3279
Satyanarayana KG, Mariano AB, Vargas JVC (2011) A review on microalgae, a versatile source for sustainable energy and materials. Int J Energy Res 35(4):291–311
Schenk PM, Thomas-Hall SR, Stephens E, Marx UC, Mussgnug JH, Posten C, Kruse O, Hankamer B (2008) Second generation biofuels: high-efficiency microalgae for biodiesel production. Bioenergy Res 1(1):20–43
Scott SA et al (2010) Biodiesel from algae: challenges and prospects. Curr Opin Biotechnol 21(3):277–286
Sharma YC, Singh B, Upadhyay SN (2008) Advancements in development and characterization of biodiesel. Fuel 87(12):2355–2373
Shiho M, Kawachi M, Horioka K, Nishita Y, Ohashi K, Kaya K, Watanabe MM (2012) Business evaluation of a green microalgae Botryococcus braunii oil production system. Innov Res Algal Biomass 15:90–109
Singh J, Cu S (2010) Commercialization potential of microalgae for biofuels production. Renew Sustain Energy Rev 14(9):2596–2610
Singh A, Nigam PS, Murphy JD (2011) Renewable fuels from algae: an answer to debatable land based fuels. Bioresour Technol 102(1):10–16
Slocombe SP, Cornah J, Pinfield-Wells H, Soady K, Zhang Q, Gilday A, Dyer JM, Graham IA (2009) Oil accumulation in leaves directed by modification of fatty acid breakdown and lipid synthesis pathways. Plant Biotechnol J 7(7):694–703
Stephenson PG, Moore CM, Terry MJ, Zubkov MV, Bibby TS (2011) Improving photosynthesis for algal biofuels: toward a green revolution. Trends Biotechnol 29(12):615–623
Stripp S, Sanganas O, Happe T, Haumann M (2009) The structure of the active site H-cluster of [FeFe] hydrogenase from the green alga Chlamydomonas reinhardtii studied by X-ray absorption spectroscopy. Biochemistry 48(22):5042–5049
Tanzi CD, Vian MA, Ginies C, Elmaataoui M, Chemat F (2012) Terpenes as green solvents for extraction of oil from microalgae. Molecules 17(7):8196–8205
Tiwari A, Pandey A (2012) Cyanobacterial hydrogen production—A step towards clean environment. Int J Hydrogen Energy 37(1):139–150
Tran DT, Chen CL, Chang JS (2012) Effect of solvents and oil content on direct transesterification of wet oil-bearing microalgal biomass of Chlorella vulgaris ESP-31 for biodiesel synthesis using immobilized lipase as the biocatalyst. Bioresour Technol (in press)
Tran HL, Hong SJ, Lee CG (2009) Evaluation of extraction methods for recovery of fatty acids from Botryococcus braunii LB 572 and Synechocystis sp. PCC 6803. Biotechnol Bioprocess Eng 14(2):187–192
Tran NH, Bartlett JR, Kannangara GSK, Milev AS, Volk H, Wilson MA (2010) Catalytic upgrading of biorefinery oil from micro-algae. Fuel 89(2):265–274
Ugwu CU, Aoyagi H, Uchiyama H (2008) Photobioreactors for mass cultivation of algae. Bioresour Technol 99(10):4021–4028
Vandamme D, Foubert I, Muylaert K (2013) Flocculation as a low-cost method for harvesting microalgae for bulk biomass production. Trends Biotechnol 31(4):233–239
Walker DA (2009) Biofuels, facts, fantasy, and feasibility. J Appl Phycol 21(5):509–517
Wanke M, Skorupinska-Tudek K, Swiezewska E (2001) Isoprenoid biosynthesis via 1-deoxy-D-xylulose 5-phosphate/2-C-methyl-D-erythritol 4-phosphate (DOXP/MEP) pathway. Acta Biochim Pol 48(3):663–672
Westerhoff P, Hu Q, Esparza-Soto M, Vermaas W (2010) Growth parameters of microalgae tolerant to high levels of carbon dioxide in batch and continuous-flow photobioreactors. Environ Technol 31(5):523–532
Wijffels RH, Barbosa MJ (2010) An outlook on microalgal biofuels. Science 329(5993):796–799
Wynn JP, Ratledge C (2005) Oils from microorganisms. In: Bailey AE, Shahidi F (eds) Bailey’s industrial oil & fat products/edited by Fereidoon Shahidi. Wiley, Hoboken, pp 121–151
Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang SG (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin: NADP+-oxidoreductase (FNR) enzymes in vitro. Proc Natl Acad Sci USA 108(23):9396–9401
Yoo C, Jun SY, Lee JY, Ahn CY, Oh HM (2010) Selection of microalgae for lipid production under high levels carbon dioxide. Bioresour Technol 101:S71–S74
Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214(4):552–561
Zheng HL, Gao Z, Yin FW, Ji XJ, Huang H (2012) Lipid production of Chlorella vulgaris from lipid-extracted microalgal biomass residues through two-step enzymatic hydrolysis. Bioresour Technol 117:1–6
Acknowledgments
This work was supported in part by a NSU President’s Faculty Research and Development Grant.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Razeghifard, R. Algal biofuels. Photosynth Res 117, 207–219 (2013). https://doi.org/10.1007/s11120-013-9828-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11120-013-9828-z