Abstract

Diversification of biofuel sources has become an important energy issue. Bio-hydrogen production from microalgae has received much attention recently. However, commercial production of microalgae biofuels including bio-hydrogen is still not feasible due to the low biomass concentration and costly downstream processes. It has been reported that exposing some species of algae to environmental stress, e.g., by depriving the algae of sulfur in light, it is possible to produce significant amounts of hydrogen gas. However, this technology is still in its infancy and there is significant potential for technology development and improvement at every level. This review discusses the biological hydrogen production by microalgae (direct bio-photolysis, indirect bio-photolysis, photo fermentation and dark fermentation) and optimization of key parameters to enhance hydrogen production. The effects of different stress reactions on production of the valuable components are described. This knowledge can be used to evaluate the possibilities for producing hydrogen and high value products efficiently in the same process. Further studies of these topics may result in a sustainable process where solar energy can be converted into hydrogen in an integrated manner, where production efficiencies are sufficient for an economic exploitation of algal technology using algal stress reactions.

Keywords:

Algal stress reactions, bio-hydrogen, hydrogenase, microalgae, microwave irradiation,

References

1. Akkerman, I., M. Janssen, J. Rocha and R.H. Wijffels, 2002. Photobiological hydrogen production: Photochemical efficiency and bioreactor design. Int. J. Hydrogen Energ., 27(11-12): 1195-1208.
   CrossRef    
2. Allakhverdiev, S., V. Thavasi, V.D. Kreslavski, S.K. Zharmukhamedov, V.V. Klimov, S. Ramakrishna, D.A. Los, M. Mimuro, H. Nishihara and R. Carpentier, 2010. Photosynthetic hydrogen production. J. Photoch. Photobio. C, 11(2-3): 101-113.
   CrossRef    
3. Asadi, A., R.A. Khavari-Nejad, N. Soltani, F. Najafi and A. Molaie-Rad, 2011. Physiological variability in cyanobacterium Phormidium sp Kutzing ISC31 (Oscillatoriales) as response to varied microwave intensities. Afr. J. Agric. Res., 6(7): 1673-1681.
   
4. Azwar, M.Y., M.A. Hussain and A.K. Abdul-Wahab, 2014. Development of biohydrogen production by photobiological, fermentation and electrochemical processes: A review. Renew. Sust. Energ. Rev., 31: 158-173.
   CrossRef    
5. Bakonyi, P., B. Borza, K. Orlovits, V. Simon, N. Nemestothy and K. Bélafi-Bakó, 2014. Fermentative hydrogen production by conventionally and unconventionally heat pretreated seed cultures: A comparative assessment. Int. J. Hydrogen Energ., 39(11): 5589-5596.
   CrossRef    
6. Banik, S., S. Bandopadhyay and S. Ganguly, 2003. Bioeffects of microwave--a brief review. Bioresource Technol., 87(2): 155-159.
   CrossRef    
7. Beckmann, J., F. Lehr, G. Finazzi, B. Hankamer, C. Posten, L. Wobbe and O. Kruse, 2009. Improvement of light to biomass conversion by de-regulation of light-harvesting protein translation in Chlamydomonas reinhardtii. J. Biotechnol., 142(1): 70-77.
   CrossRef    PMid:19480949    
8. Burrows, E.H., F.W.R. Chaplen and R.L. Ely, 2008. Optimization of media nutrient composition for increased photofermentative hydrogen production by Synechocystis sp. PCC 6803. Int. J. Hydrogen Energ., 33(21): 6092-6099.
   CrossRef    
9. Carvalho, A.P., L.A. Meireles and F.X. Malcata, 2006. Microalgal reactors: A review of enclosed system designs and performances. Biotechnol. Progr., 22(6): 1490-1506.
   CrossRef    PMid:17137294    
10. Chandrasekhar, K., Y.J. Lee and D.W. Lee, 2015. Biohydrogen production: Strategies to improve process efficiency through microbial routes. Int. J. Mol. Sci., 16(4): 8266-8293.
    CrossRef    PMid:25874756 PMCid:PMC4425080    
11. Chen, C.Y., W.B. Lu, J.F. Wu and J.S. Chang, 2007. Enhancing phototrophic hydrogen production of Rhodopseudomonas palustris via statistical experimental design. Int. J. Hydrogen Energ., 32(8): 940-949.
    CrossRef    
12. Chisti, Y., 2007. Biodiesel from microalgae. Biotechnol. Adv., 25(3): 294-306.
    CrossRef    PMid:17350212    
13. Chung, I.K., J. Beardall, S. Mehta, D. Sahoo and S. Stojkovic, 2011. Using marine macroalgae for carbon sequestration: A critical appraisal. J. Appl. Phycol., 23(5): 877-886.
    CrossRef    
14. Das, D. and T.N. Veziroglu, 2001. Hydrogen production by biological processes: A survey of literature. Int. J. Hydrogen Energ., 26(1): 13-28.
    CrossRef    
15. Das, D. and T.N. Veziroglu, 2008. Advances in biological hydrogen production processes. Int. J. Hydrogen Energ., 33(21): 6046-6057.
    CrossRef    
16. Dasgupta, C.N., J.J. Gilberta, P. Lindblad, T. Heidorn, S.A. Borgvang, K. Skjanes and D. Das, 2010. Recent trends on the development of photobiological processes and photobioreactors for the improvement of hydrogen production. Int. J. Hydrogen Energ., 35(19): 10218-10238.
    CrossRef    
17. Erbes, D.L., D. King and M. Gibbs, 1979. Inactivation of hydrogenase in cell-free extracts and whole cells of Chlamydomonas reinhardi by oxygen. Plant Physiol., 63(6): 1138-1142.
    CrossRef    PMid:16660871 PMCid:PMC542984    
18. Eroglu, E. and A. Melis, 2011. Photobiological hydrogen production: Recent advances and state of the art. Bioresource Technol., 102(18): 8403-8413.
    CrossRef    PMid:21463932    
19. Fabiano, B. and P. Perego, 2002. Thermodynamic study and optimization of hydrogen production by Enterobacter aerogenes. Int. J. Hydrogen Energ., 27(2): 149-156.
    CrossRef    
20. Fang, H.H.P., H. Zhu and T. Zhang, 2006. Phototrophic hydrogen production from glucose by pure and co-cultures of Clostridium butyricum and Rhodobacter sphaeroides. Int. J. Hydrogen Energ., 31(15): 2223-2230.
    CrossRef    
21. Ferchichi, M., E. Crabbe, G.H. Gil, W. Hintz and A. Almadidy, 2005. Influence of initial pH on hydrogen production from cheese whey. J. Biotechnol., 120(4): 402-409.
    CrossRef    PMid:16242202    
22. Ghirardi, M.L., L. Zhang, J.W. Lee, T. Flynn, M. Seibert, E. Greenbaum and A. Melis, 2000. Microalgae: A green source of renewable H(2). Trends Biotechnol., 18(12): 506-511.
    CrossRef    
23. Ghirardi, M.L., P. King, S. Kosourov, M. Forestier, L. Zhang and M. Seibert, 2006. Development of Algal Systems for Hydrogen Photoproduction: Addressing the Hydrogenase Oxygen-Sensitivity Problem. In: Collings, A.F. and C. Critchley (Eds.), Artificial Photosynthesis: From Basic Biology to Industrial Application. Wiley-VCH Verlag GmbH & Co., Weinheim, pp: 213-227.
    CrossRef    
24. Gressler, P., R. Schneider, V. Corbellini, T. Bjerk, M. Souza, A. Zappe and E.A. Lobo, 2012. Microalgas: Aplicações em biorremediação e energia. In English: Microalgae: Aplications in bioremediation and energy. Cad. Pesquisa Sér. Biol., 24(1): 48-67.
    
25. Guan, Y., M. Deng, X. Yu and W. Zhang, 2004. Two-stage photo-biological production of hydrogen by marine green alga Platymonas subcordiformis. Biochem. Eng. J., 19(1): 69-73.
    CrossRef    
26. Gutierrez-Wing, M.T., A. Silaban, J. Barnett and K.A. Rusch, 2014. Light irradiance and spectral distribution effects on microalgal bioreactors. Eng. Life Sci., 14(6): 574-580.
    CrossRef    
27. Gutthann, F., M. Egert, A. Marques and J. Appel, 2007. Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. Biochim. Biophys. Acta, 1767(2): 161-169.
    
28. Hahn, J.J., M.L. Ghirardi and W.A. Jacoby, 2007. Immobilized algal cells used for hydrogen production. Biochem. Eng. J., 37(1): 75-79.
    CrossRef    
29. Hallenbeck, P.C. and J.R. Benemann, 2002. Biological hydrogen production; fundamentals and limiting processes. Int. J. Hydrogen Energ., 27(11-12): 1185-1193.
    CrossRef    
30. Herrero, M.A., J.M. Kremsner and C.O. Kappe, 2008. Nonthermal microwave effects revisited: On the importance of internal temperature monitoring and agitation in microwave chemistry. J. Org. Chem., 73(1): 36-47.
    CrossRef    PMid:18062704    
31. Hsia, S.Y. and Y.T. Chou, 2014. Optimization of biohydrogen production with biomechatronics. J. Nanomater., 2014: 1-11.
    CrossRef    
32. Jeberlin Prabina, B. and K. Kumar, 2010. Studies on the optimization of cultural conditions for maximum hydrogen production by selected cyanobacteria. ARPN J. Agric. Biol. Sci., 5(5): 22-31.
    
33. Jo, J.H., D.S. Lee and J.M. Park, 2006. Modeling and optimization of photosynthetic hydrogen gas production by green alga Chlamydomonas reinhardtii in sulfur-deprived circumstance. Biotechnol. Progr., 22(2): 431-437.
    CrossRef    PMid:16599558    
34. Johnston, B., M.C. Mayo and A. Khare, 2005. Hydrogen: The energy source for the 21st century. Technovation, 25(6): 569-585.
    CrossRef    
35. Kars, G., U. Gündüz, M. Yücel, L. Türker and I. Eroglu, 2006. Hydrogen production and transcriptional analysis of nifD, nifK and hupS genes in Rhodobacter sphaeroides O.U.001 grown in media with different concentrations of molybdenum and iron. Int. J. Hydrogen Energ., 31(11): 1536-1544.
    CrossRef    
36. Karthic, P. and J. Shiny, 2012. Comparisons and limitations of biohydrogen production processes. Res. J. Biotechnol., 7(2): 59-71.
    
37. Keskin, T., L. Giusti and N. Azbar, 2012. Continuous biohydrogen production in immobilized biofilm system versus suspended cell culture. Int. J. Hydrogen Energ., 37(2): 1418-1424.
    CrossRef    
38. Kilonzo, P. and M. Bergougnou, 2012. Surface modifications for controlled and optimized cell immobilization by adsorption: Applications in fibrous bed bioreactors containing recombinant cells. J. Microbial Biochem. Technol., S8(1): 1-9.
    CrossRef    
39. Kim, D.H. and M.S. Kim, 2011. Hydrogenases for biological hydrogen production. Bioresource Technol., 102(18): 8423-8431.
    CrossRef    PMid:21435869    
40. Kim, J.P., C.D. Kang, T.H. Park, M.S. Kim and S.J. Sim, 2006. Enhanced hydrogen production by controlling light intensity in sulfur-deprived Chlamydomonas reinhardtii culture. Int. J. Hydrogen Energ., 31(11): 1585-1590.
    CrossRef    
41. Koku, H., I. Eroglu, U. Gündüz, M. Yücel and L. Türker, 2003. Kinetics of biological hydrogen production by the photosynthetic bacterium Rhodobacter sphaeroides O.U. 001. Int. J. Hydrogen Energ., 28(4): 381-388.
    CrossRef    
42. Kosourov, S., M. Seibert and M.L. Ghirardi, 2003. Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures. Plant Cell Physiol., 44(2): 146-155.
    CrossRef    PMid:12610217    
43. Kosourov, S.N. and M. Seibert, 2009. Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions. Biotechnol. Bioeng., 102(1): 50-58.
    CrossRef    PMid:18823051    
44. Kotay, S.M. and D. Das, 2007. Microbial hydrogen production with Bacillus coagulans IIT-BT S1 isolated from anaerobic sewage sludge. Bioresource Technol., 98(6): 1183-1190.
    CrossRef    PMid:16797976    
45. Kothari, A., 2013. Improving cyanobacterial hydrogen production through bioprospecting of natural microbial communities. Ph.D. Thesis, Department of Molecular and Cellular Biology, Arizona State University, pp: 268.
    
46. Kumar, A., S. Ergas, X. Yuan, A. Sahu, Q. Zhang, J. Dewulf, F. Xavier Malcata and H. van Langenhove, 2010. Enhanced CO2 fixation and biofuel production via microalgae: Recent developments and future directions. Trends Biotechnol., 28(7): 371-380.
    CrossRef    PMid:20541270    
47. Kumar, N. and D. Das, 2000. Enhancement of hydrogen production by Enterobacter cloacae IIT-BT 08. Process Biochem., 35(6): 589-593.
    CrossRef    
48. Kumazawa, S. and A. Mitsui, 1981. Characterization and optimization of hydrogen photoproduction by a saltwater blue-green alga, Oscillatoria sp. Miami BG7. I. Enhancement through limiting the supply of nitrogen nutrients. Int. J. Hydrogen Energ., 6(4): 339-348.
    CrossRef    
49. Lai, W.H., H.Y. Chen, F.Y. Chang, C.C. Wu, C.Y. Lin and S.R. Huang, 2011. Market and patent analysis of commercializing biohydrogen technology. Int. J. Hydrogen Energ., 36: 14049-14058.
    CrossRef    
50. Laurinavichene, T.V., A.S. Fedorov, M.L. Ghirardi, M. Seibert and A.A. Tsygankov, 2006. Demonstration of sustained hydrogen photoproduction by immobilized, sulfur-deprived Chlamydomonas reinhardtii cells. Int. J. Hydrogen Energ., 31(5): 659-667.
    CrossRef    
51. Lazaro, C.Z., M.B.A. Varesche and E.L. Silva, 2015. Effect of inoculum concentration, pH, light intensity and lighting regime on hydrogen production by phototrophic microbial consortium. Renew. Energ., 75: 1-7.
    CrossRef    
52. Lee, D.H. and L.H. Chiu, 2012. Development of a biohydrogen economy in the United States, China, Japan, and India: With discussion of a chicken-and-egg debate. Int. J. Hydrogen Energ., 37(20): 15736-15745.
    CrossRef    
53. Lemus, R.G. and J.M.M. Duart, 2010. Updated hydrogen production costs and parities for conventional and renewable technologies. Int. J. Hydrogen Energ., 35(9): 3929-3936.
    CrossRef    
54. Le Quéré, C., R.J. Andres, T. Boden, T. Conway, R.A. Houghton, J.I. House, G. Marland, G.P. Peters, G. van der Werf, A. Ahlström, R.M. Andrew, L. Bopp, J.G. Canadell, P. Ciais, S.C. Doney, C. Enright, P. Friedlingstein, C. Huntingford, A.K. Jain, C. Jourdain, E. Kato, R.F. Keeling, K. Klein Goldewijk, S. Levis, P. Levy, M. Lomas, B. Poulter, M.R. Raupach, J. Schwinger, S. Sitch, B.D. Stocker, N. Viovy, S. Zaehle and N. Zeng, 2012. The global carbon budget 1959-2011. Earth Syst. Sci. Data Discuss., 5(2): 1107-1157.
    CrossRef    
55. Levin, D.B., L. Pitt and M. Love, 2004. Biohydrogen production: Prospects and limitations to practical application. Int. J. Hydrogen Energ., 29(2): 173-185.
    CrossRef    
56. Lewis, N.S. and D.G. Nocera, 2006. Powering the planet: Chemical challenges in solar energy utilization. P. Natl. Acad. Sci. USA, 103(43): 15729-15735.
    CrossRef    PMid:17043226 PMCid:PMC1635072    
57. Lin, C.Y. and C.H. Jo, 2003. Hydrogen production from sucrose using an anaerobic sequencing batch reactor process. J. Chem. Technol. Biot., 78(6): 678-684.
    CrossRef    
58. Liu, J., V.E. Bukatin and A.A. Tsygankov, 2006. Light energy conversion into H2 by Anabaena variabilis mutant PK84 dense cultures exposed to nitrogen limitations. Int. J. Hydrogen Energ., 31(11): 1591-1596.
    CrossRef    
59. Maniatis, K., 2003. Pathways for the Production of Bio-hydrogen: Opportunities and Challenges. In: Towards Hydrogen. IEA, Paris.
    
60. Manish, S. and R. Banerjee, 2008. Comparison of biohydrogen production processes. Int. J. Hydrogen Energ., 33(1): 279-286.
    CrossRef    
61. Mathews, J. and G. Wang, 2009. Metabolic pathway engineering for enhanced biohydrogen production. Int. J. Hydrogen Energ., 34(17): 7404-7416.
    CrossRef    
62. Melis, A., 2002. Green alga hydrogen production: Progress, challenges and prospects. Int. J. Hydrogen Energ., 27(11-12): 1217-1228.
    CrossRef    
63. Melis, A., 2007. Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta, 226(5): 1075-1086.
    CrossRef    PMid:17721788    
64. Melis, A. and T. Happe, 2001. Hydrogen production. Green algae as a source of energy. Plant Physiol., 127(3): 740-748.
    CrossRef    PMid:11706159 PMCid:PMC1540156    
65. Melis, A., L. Zhang, M. Forestier, M.L. Ghirardi and M. Seibert, 2000. Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol., 122(1): 127-136.
    CrossRef    PMid:10631256 PMCid:PMC58851    
66. Mishra, T., P. Kushwah, K. Dholiya and V. Kothari, 2013. Effect of low power microwave radiation on microorganisms and other life forms. AMWT, 1(1): 4.
    CrossRef    
67. Momirlan, M. and T.N. Veziroglu, 2005. The properties of hydrogen as fuel tomorrow in sustainable energy system for a cleaner planet. Int. J. Hydrogen Energ., 30(7): 795-802.
    CrossRef    
68. Mussgnug, J.H., S. Thomas-Hall, J. Rupprecht, A. Foo, V. Klassen, A. McDowall, P.M. Schenk, O. Kruse and B. Hankamer, 2007. Engineering photosynthetic light capture: Impacts on improved solar energy to biomass conversion. Plant Biotechnol. J., 5(6): 802-814.
    CrossRef    PMid:17764518    
69. Nath, K., A. Kumar and D. Das, 2006. Effect of some environmental parameters on fermentative hydrogen production by Enterobacter cloacae DM11. Can. J. Microbiol., 52(6): 525-532.
    CrossRef    PMid:16788720    
70. Nath, K. and D. Das, 2011. Modeling and optimization of fermentative hydrogen production. Bioresource Technol., 102(18): 8569-8581.
    CrossRef    PMid:21531132    
71. Oh, Y.K., E.H. Seol, J.R. Kim and S. Park, 2003. Fermentative biohydrogen production by a new chemoheterotrophic bacterium Citrobacter sp. Y19. Int. J. Hydrogen Energ., 28(12): 1353-1359.
    CrossRef    
72. Olivo, C., I. Lebedeva, C.Y. Chu, C.Y. Lin and S.Y. Wu, 2011. A patent analysis on advanced biohydrogen technology development and commercialisation: Scope and competitiveness. Int. J. Hydrogen Energ., 36: 14103-14110.
    CrossRef    
73. Oncel, S. and F. Vardar Sukan, 2011. Effect of light intensity and the light: Dark cycles on the long term hydrogen production of Chlamydomonas reinhardtii by batch cultures. Biomass Bioenerg., 35(3): 1066-1074.
    CrossRef    
74. Öztürk, Y., M. Yücel, F. Daldal, S. Mandaci, U. Gündüz, L. Türker and I. Eroglu, 2006. Hydrogen production by using Rhodobacter capsulatus mutants with genetically modified electron transfer chains. Int. J. Hydrogen Energ., 31(11): 1545-1552.
    CrossRef    
75. Pelczar, Jr. M.J., E.C.S. Chan and N.R. Krieg, 2008. Microbiology Concepts and Application. 2nd Edn., Pearson Makron Books.
    PMCid:PMC2519376    
76. Polle, J.E.W., J.R. Benemann, A. Tanaka and A. Melis, 2000. Photosynthetic apparatus organization and function in the wild type and a chlorophyll b-less mutant of Chlamydomonas reinhardtii. Dependence on carbon source. Planta, 211(3): 335-344.
    CrossRef    PMid:10987551    
77. Polle, J.E.W., S. Kanakagiri, E. Jin, T. Masuda and A. Melis, 2002. Truncated chlorophyll antenna size of the photosystems—a practical method to improve microalgal productivity and hydrogen production in mass culture. Int. J. Hydrogen Energ., 27(11-12): 1257-1264.
    CrossRef    
78. Polle, J.E., S.D. Kanakagiri and A. Melis, 2003. Tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta, 217(1): 49-59.
    PMid:12721848    
79. Prince, R.C. and H.S. Kheshgi, 2005. The photobiological production of hydrogen: Potential efficiency and effectiveness as a renewable fuel. Crit. Rev. Microbiol., 31(1): 19-31.
    CrossRef    PMid:15839402    
80. Quadrelli, R. and S. Peterson, 2007. The energy–climate challenge: Recent trends in CO2 emissions from fuel combustion. Energ. Policy, 35(11): 5938-5952.
    CrossRef    
81. Rajeshwar, K., R. McConnell, K. Harrison and S. Licht, 2008. Renewable Energy and the Hydrogen Economy. In: Rajeshwar, K., R. McConnell and S. Lich (Eds.), Solar Hydrogen Generation: Toward a Renewable Energy Future. Springer, New York, pp: 1-18.
    CrossRef    
82. Rashid, N., K. Lee and Q. Mahmood, 2011. Bio-hydrogen production by Chlorella vulgaris under diverse photoperiods. Bioresource Technol., 102(2): 2101-2104.
    CrossRef    PMid:20826084    
83. Rashid, N., M.S.U. Rehman, S. Memon, Z. Ur Rahman, K. Lee and J.I. Han, 2013. Current status, barriers and developments in biohydrogen production by microalgae. Renew. Sust. Energ. Rev., 22: 571-579.
    CrossRef    
84. Rashid, N., W. Song, J. Park, H.F. Jin and K. Lee, 2009. Characteristics of hydrogen production by immobilized cyanobacterium Microcystis aeruginosa through cycles of photosynthesis and anaerobic incubation. J. Ind. Eng. Chem., 15(4): 498-503.
    CrossRef    
85. Razeghifard, R., 2013. Algal biofuels. Photosynth. Res., 117(1-3): 207-219.
    CrossRef    PMid:23605290    
86. Rupprecht, J., B. Hankamer, J.H. Mussgnug, G. Ananyev, C. Dismukes and O. Kruse, 2006. Perspectives and advances of biological H2 production in microorganisms. Appl. Microbiol. Biot., 72(3): 442-449.
    CrossRef    PMid:16896600    
87. Sambusiti, C., M. Bellucci, A. Zabaniotou, L. Beneduce and F. Monlau, 2015. Algae as promising feedstocks for fermentative biohydrogen production according to a biorefinery approach: A comprehensive review. Renew. Sust. Energ. Rev., 44: 20-36.
    CrossRef    
88. Shaishav, S., R.N. Singh and T. Satyendra, 2013. Biohydrogen from algae: Fuel of the future. Int. Res. J. Environ. Sci., 2(4): 44-47.
    
89. Show, K.Y., D.J. Lee, J.H. Tay, C.Y. Lin and J.S. Chang, 2012. Biohydrogen production: Current perspectives and the way forward. Int. J. Hydrogen Energ., 37(20): 15616-15631.
    CrossRef    
90. Srirangan, K., M.E. Pyne and C. Perry Chou, 2011. Biochemical and genetic engineering strategies to enhance hydrogen production in photosynthetic algae and cyanobacteria. Bioresource Technol., 102(18): 8589-8604.
    CrossRef    PMid:21514821    
91. Stripp, S.T. and T. Happe, 2009. How algae produce hydrogen--news from the photosynthetic hydrogenase. Dalton T., 45: 9960-9969.
    CrossRef    PMid:19904421    
92. Troshina, O., L. Serebryakova, M. Sheremetieva and P. Lindblad, 2002. Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. Int. J. Hydrogen Energ., 27(11-12): 1283-1289.
    CrossRef    
93. Tsygankov, A.A., S.N. Kosourov, I.V. Tolstygina, M.L. Ghirardi and M. Seibert, 2006. Hydrogen production by sulfur-deprived Chlamydomonas reinhardtii under photoautotrophic conditions. Int. J. Hydrogen Energ., 31(11): 1574-1584.
    CrossRef    
94. Uggetti, E., B. Sialve, E. Trably and J.P. Steyer, 2014. Integrating microalgae production with anaerobic digestion: A biorefinery approach. Biofuel. Bioprod. Bior., 8(4): 516-529.
    CrossRef    
95. Uyar, B., I. Eroglu, M. Yücel, U. Gündüz and L. Türker, 2007. Effect of light intensity, wavelength and illumination protocol on hydrogen production in photobioreactors. Int. J. Hydrogen Energ., 32(18): 4670-4677.
    CrossRef    
96. Vardar-Schara, G., T. Maeda and T.K. Wood, 2008. Metabolically engineered bacteria for producing hydrogen via fermentation. Microb. Biotechnol., 1(2): 107-125.
    CrossRef    PMid:21261829 PMCid:PMC3864445    
97. Vignais, P.M., 2008. Hydrogenases and H(+)-reduction in primary energy conservation. Results Probl. Cell Differ., 45: 223-252.
    CrossRef    PMid:18500479    
98. Wahal, S. and S. Viamajala, 2010. Maximizing algal growth in batch reactors using sequential change in light intensity. Appl. Biochem. Biotech., 161(1-8): 511-522.
    
99. White, A.L. and A. Melis, 2006. Biochemistry of hydrogen metabolism in Chlamydomonas reinhardtii wild type and a Rubisco-less mutant. Int. J. Hydrogen Energ., 31(4): 455-464.
    CrossRef    
100. Winkler, M., A. Hemschemeier, C. Gotor, A. Melis and T. Happe, 2002. [Fe]-hydrogenases in green algae: Photo-fermentation and hydrogen evolution under sulfur deprivation. Int. J. Hydrogen Energ., 27(11-12): 1431-1439.
     CrossRef    
101. Wu, S., X. Li, J. Yu and Q. Wang, 2012. Increased hydrogen production in co-culture of Chlamydomonas reinhardtii and Bradyrhizobium japonicum. Bioresource Technol., 123: 184-188.
     CrossRef    PMid:22940317    
102. Younesi, H., G. Najafpour, K.S. Ku Ismail, A.R. Mohamed and A.H. Kamaruddin, 2008. Biohydrogen production in a continuous stirred tank bioreactor from synthesis gas by anaerobic photosynthetic bacterium: Rhodopirillum rubrum. Bioresource Technol., 99(7): 2612-2619.
     CrossRef    PMid:17582763    
103. Zhang, H., M.A. Bruns and B.E. Logan, 2006. Biological hydrogen production by Clostridium acetobutylicum in an unsaturated flow reactor. Water Res., 40(4): 728-734.
     CrossRef    PMid:16427113    
104. Zhang, L., M. He and J. Liu, 2014. The enhancement mechanism of hydrogen photoproduction in Chlorella protothecoides under nitrogen limitation and sulfur deprivation. Int. J. Hydrogen Energ., 39(17): 8969-8976.
     CrossRef    
105. Zhang, L., T. Happe and A. Melis, 2002. Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta, 214(4): 552-561.
     CrossRef    PMid:11925039    
106. Zhu, L.D., E. Hiltunen, E. Antila, J.J. Zhong, Z.H. Yuan and Z.M. Wang, 2014. Microalgal biofuels: Flexible bioenergies for sustainable development. Renew. Sust. Energ. Rev., 30: 1035-1046.
     CrossRef    

Competing interests

The authors have no competing interests.

Open Access Policy

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Copyright

The authors have no competing interests.