Abstract
Biological hydrogen production from microbial origins especially from microalgal species has been an attractive source for the world to compensate the extreme fuel consumption of civilized population. The attribution of biohydrogen production is thought to be effective on macroscale considering global energy market; however there exist lots of biochemical reactions in a single cell to produce hydrogen. From this point of view, the aim of this chapter is to highlight the enzymes responsible for biohydrogen production in microalgae and to discuss enzymatic reactions focusing on cell dynamics, metabolism, structure, function, and challenges regarding sustainable biohydrogen production.
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References
Adams MWW (1990) The structure and mechanism of iron hydrogenases. Biochim Biophys Acta 1020:115–145
Antal TK, Krendeleva TE, Laurinavichene TV, Makarova VV, Ghirardi ML, Rubin AB, Tsygangov AA, Seibert M (2003) The dependence of algal H2 production on photosystem II and O2 consumption in sulfur-deprived Chlamydomonas reinhardtii cells. BBA 1607:153–160
Antal TK, Krendeleva TE, Rubin AB (2011) Acclimation of green algae to sulfur deficiency: underlying mechanisms and application for hydrogen production. Appl Microbiol Biotechnol 89:3–15
Aparico PJ, Azuara MP, Antonio B, Fernandez VM (1985) Effect of light intensity and oxidized nitrogen sources on hydrogen production by Chlamydomonas reinhardtii. Plant Physiol 78:803–806
Apte SK, Prabhavathi N (1994) Reaaragements of nitrogen fixation (nif) genes in heterocystous cyanobacteria. Bioscience 19(5):579–602
Baebprasert W, Jantaro S, Khetkorn W, Lindblad P, Incharoensakdi A (2011) Increased H2 production in the cyanobacterium Synechocystis sp. strain PCC6803 by redirecting the electron supply via genetic engineering of the nitrate assimilation pathway. Metab Eng 13(5):610–616
Barz M, Beimgraben C, Staller T, Germer F, Opitz F, Marquardt C, Schwarz C, Gutekunst K, Vanselow KH, Schmitz R, LaRoche J, Schulz R, Appel J (2010) Distribution analysis of hydrogenases in surface waters of marine and freshwater environments. PLoS One 5:13849
Beer LL, Boyd ES, Peters JW, Posewitz MC (2009) Engineering algae for biohydrogen and biofuel production. Curr Opin Biotechnol 20:264–271
Belay A (2013) Biology and industrial production of Arthrospira (Spirulina). Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, West Sussex, pp 339–358
Benemann JR (1997) Feasibility analysis of photobiological hydrogen production. Int J Hydrog Energy 22(10/11):979–987
Berggren G, Adamska A, Lambertz C, Simmons TR, Esselborn J, Attal M, Gambarelli S, Mouesca JM, Reijerse E, Lubitz W, Happe T, Artero V, Fontecave M (2013) Biomimetic assembly and activation of [FeFe]-hydrogenases. Nature 499:66–70
Bergman B, Carpenter EJ (1991) Nitrogenase confined to randomly distributed trichomes in the marine cyanobacterium Trichodesmium thiebautii. J Phycol 27:158–165
Bishop NI, Gaffron H (1963) photoreduction at λ705 mμ in adapted algae. Biochem Biophys Res Commun 8:471–476
Blaby IK, Blaby Haas CE, Tourasse N, Hom EFY, Lopez D, Aksoy M, Grossman A et al (2014) The Chlamydomonas genome project: a decade on. Trends Biotechnol 19(10):672–680
Bochenek M, Etherington GJ, Koprivova A, Mugford ST, Bell TG, Malin G, Kopriva S (2013) Transcriptome analysis of the sulfate deficiency response in the marine microalgae Emiliania huxleyi. New Phytol 199:650–662
Borowitzka AM (2013) Energy from microalgae: a short history. In: Borowitzka MA, Moheimani NR (eds) Algae for biofuels and energy. Springer, Dordrecht, pp 1–15
Bui ETN, Johnson PJ (1996) Identification and characterization of [Fe]-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol Biochem Parasitol 76(1–2):305–310
Cao X, Wu X, Ji C, Yao C, Chen Z, Li G, Xue S (2008) Comparative transcriptional study on the hydrogen evolution of marine microalga Tetraselmis subcordiformis. Biochim Biophys Acta 1777:410–416
Carrieri D, Wawrousek K, Eckert C, Yu J, Maness PJ (2011) The role of bidirectional hydrogenases in cyanobacteria. Bioresour Technol 102:8368–8377
Casalot L, Rousset M (2001) Maturation of [NiFe] hydrogenases. Trends Microbiol 9(5):228–237
Cavazza C, Martin L, Mondy S, Gaillard J, Rater P, Fontecilla-Camps JC (2008) The possible role of an [FeFe]-hydrogenase-like protein in the plant responses to changing atmospheric oxygen levels. J Inorg Biochem 102:1359–1365
Chen HC, Melis A (2004) Localization and function of SulP, a nuclear encoded chloroplast sulfate permease in Chlamydomonas reinhardtii. Planta 220(2):198–210
Chen M, Zhao L, Sun YL, Cui SX, Zhang LF, Yang B, Wang J, Kuang TY, Huang F (2010) Proteomic analysis of hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. J Proteome Res 9:3854–3866
Chenevier P, Mugherli L, Darbe S, Darchy L, Dimanno S, Tran PD, Valentino F, Iannello M, Volbeda A, Cavazza C, Artero V (2013) Hydrogenase enzymes: application in biofuel cells and inspiration for the design of noble-metal free catalysts for H2 oxidation. R Chim 16:491–505
Chochois V, Dauvillée D, Beyly A, Tolleter D, Cuiné S, Timpano H, Ball S, Cournac L, Peltier G (2009) Hydrogen production in Chlamydomonas, photosystem II-dependent and-independent pathways differ in their requirement for starch metabolism. Plant Physiol 151:631–640
Corr MJ, Murphy JA (2011) Evolution in the understanding of [Fe]-hydrogenase. Chem Soc Rev 40:2279–2292
Dickson DJ, Page CJ, Ely RL (2009) Photobiological hydrogen production from Synechocystis sp. PCC 6803 encapsulated in silica sol gel. Int J Hydrog Energy 34:204–215
Doebbe A, Rupprecht J, Beckmann J, Mussgnug JH, Hallmann A, Hankamer B, Kruse O (2007) Functional integration of the HUP1 hexose symporter gene into the genome of C. reinhardtii, impacts on biological H2 production. J Biotechnol 131(1):27–33
Dos Santos PC, Igarashi RY, Lee HI, Hoffman BM, Seefeldt LC, Dean DR (2005) Substrate interactions with the nitrogenase active site. Acc Chem Res 38:208–214
Faraloni C, Torzillo G (2010) Phenotypic characterization and hydrogen production in Chlamydomonas reinhardtii QB binding D1 protein mutants under sulfur starvation, changes in chlorophyll fluorescence and pigment composition. J Phycol 46:788–799
Fedorov AS, Kosourov S, Ghirardi MI, Seibert M (2005) Continuous hydrogen photoproduction by Chlamydomonas reinhardtii using a novel two-stage, sulfate-limited chemostat system. Appl Biochem Biotechnol 121:403–412
Finazzi G, Furia A, Barbagallo RM, Forti G (1999) State transitions, cyclic and linear transport and photophorylation in Chlamydomonas reinhardtii. BBA 1413:117–129
Florence M, Dubini A, Seibert M, Posewitz MC, Grossman AR (2007) Anaerobic acclimation in Chlamydomonas reinhardtii: anoxic gene expression, hydrogenase induction, and metabolic pathways. J Biol Chem 282:25475–25486
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 276:6125–6132
Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270:2750–2758
Friedrich B, Buhrke T, Burgdorf T, Lenz O (2005) A hydrogen-sensing multiprotein complex controls aerobic hydrogen metabolism in Ralstonia eutropha. Biochem Soc Trans 33:97–101
Gaffron H (1944) Photosynthesis photoreduction and dark reduction of carbon dioxide in certain algae. Biol Rev Camb Phil Soc 19:1–20
Gaffron H, Rubin J (1942) Fermentative and photochemical production of hydrogen in algae. J Gen Physiol 26:219–240
Ghirardi M, Mohanty P (2010) Oxygenic hydrogen production- current status of the technology. Curr Sci India 98:499–507
Ghirardi ML, Togasaki R, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63–65:141–151
Ghirardi ML, Zhang L, Lee JW, Flynn T, Seibert M, Greenbaum E, Melis A (2000) Microalgae, a green source of renewable H2. TIBTECH 18:506–511
Ghirardi ML, Cohen J, King P, Schulten K, Kim K, Seibert M (2006) [FeFe]-hydrogenases and photobiological hydrogen production. SPIE 6340:U257–U262
Giannelli L, Torzillo G (2012) Hydrogen production with the microalga Chlamydomonas reinhardtii grown in a compact tubular photobioreactor immersed in a scattering light nanoparticle suspension. Int J Hydrog Energy 37:16951–16961
Gibbs M, Gfeller RP, Chen C (1986) Fermentative metabolism of Chlamydomonas reinhardtii: III. Photoassimilation of acetate. Plant Physiol 82:160–166
Gimpel JA, Specht EA, Georgianna DR, Mayfield SP (2013) Advances in microalgae engineering and synthetic biology applications for biofuel production. Curr Opin Biotechnol 17:489–495
Ginovska-Pangovska B, Ho MH, Linehan JC, Cheng Y, Dupuis M, Raugei S, Shaw W (2014) Molecular dynamics study of the proposed proton transfer pathways in [FeFe] hydrogenase. Biochim Biophys Acta 1873:131–138
Girbal L, von Abendroth G, Winkler M, Benton PMC, Meynial-Salles I, Croux C et al (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 71:2777–2781
Godaux D, Emonds-Alta B, Berne N, Ghysels B, Alric J, Remacle C, Cardol P (2013) A novel screening method for hydrogenase-deficient mutants in Chlamydomonas reinhardtii based on in vivo chlorophyll fluorescence and photosystem II quantum yield. Int J Hydrog Energy 38:1826–1836
Godman JE, Molnar A, Baulcombe DC, Bakl J (2010) RNA silencing of hydrogenase-like genes and investigation of their physiological roles in the green alga Chlamydomonas reinhardtii. BioChem J 431:345–351
Gomes de Oliviera Dal’Molin C, Quek LE, Palfreyman RW, Nielsen LK (2011) AlgaGEM – a genome-scale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome. BMC Genomics 12(4):5
Greenbaum E (1982) Photosynthetic hydrogen and oxygen production: kinetic studies. Science 196:879–880
Greenbaum E, Guillard RRL, Sunda WG (1983) Hydrogen and oxygen photoproduction by marine algae. Photochem Photobiol 37:649–655
Greening C, Cook GM (2014) Integration of hydrogenase expression and hydrogen sensing in bacterial cell physiology. Curr Opin Microbiol 18:30–38
Grossman AR (2000) Acclimation of Chlamydomonas reinhardtii to its nutrient environment. Protist 151:201–224
Grossman AR (2005) Paths toward algal genomics. Plant Physiol 137:410–427
Guaernieri MT, Pienkos PT (2013) Algal omics: unlocking bioproduct diversity in algae cell factories. Photosynth Res. doi:10.1007/s11120-014-9989-4
Guan Y, Deng M, Yu X, Zhang W (2004) Two-stage photo-biological production of hydrogen by marine green alga Platymonas subcordiformis. Biochem Eng J 19:69–73
Gugger MF, Hoffmann L (2004) Polyphyly of the true branching cyanobacterial (stigonematales). Int J Syst Evol Microsc 54:349–357
Gust D, Moore TA, Moore AL (2009) Solar fuels via artificial photosynthesis. Acc Chem Res 42(12):1890–1898
Hallenbeck PC (2011) Hydrogen production by cyanobacteria. In: Hallenbeck PC (ed) Microbial technologies at advanced biofuel production. Springer US, Boston, pp 15–28
Hallenbeck PC, Abo-Hashesh M, Ghosh D (2012) Strategies for improving biological hydrogen production. Bioresour Technol 110:1–9
Hambourger M, Gervaldo M, Svedruzic D, King PW, Gust D, Ghirardi M, Moore AL, Moore TA (2008) [FeFe]-hydrogenase-catalyzed H2 production in a photoelectrochemical. Biofuels Cell J Am Chem Soc 130:2015–2022
Happe T, Hemsheimer A (2011) Metalloprotein mimics –old tools in a new light. Trends Biotechnol 32(4):170–176
Happe T, Kaminski A (2002) Differential regulation of the Fe hydrogenase during anaerobic adaptation in the green alga Chlamydomonas reinhardtii. Eur J Biochem 269:1022–1032
Happe T, Naber JD (2003) Isolation, characterization and N-terminal amino acid sequence of hydrogenase from the green alga Chlamydomonas reinhardtii. Eur J Biochem 214:475–481
Happe T, Mosler B, Naber JD (1994) Induction, localization and metal content of hydrogenase in the green alga Chlamydomonas reinhardtii. Eur J Biochem 222:769–774
Healey FP (1970) Hydrogen evolution by microalgae. Planta (Berl) 91:220–226
Heinekey MD (2009) Hydrogenase enzymes: recent structural studies and active site models. J Organomet Chem 694:2671–2680
Hemaiswarya S, Raja R, Ravikumar R, Carvalho IS (2013) Mechanism of Action of Probiotics. Braz Arch Biol Technol 56:113–119
Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926
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 227:397–407
Hoffman BM, Lukoyanov D, Dean DR, Seefeldt LC (2013) Nitrogenase: a draft mechanism Acc. Chem Res 46(2):587–595
Horch M, Lauterbach L, Lenz O, Hildebrandt P, Zebger I (2012) NAD(H)-coupled hydrogen cycling – structure–function relationships of bidirectional [NiFe] hydrogenases. FEBS Lett 586:545–556
Horner DS, Heil B, Happe T, Embley TM (2002) Iron hydrogenases-ancient enzymes in modern eukaryotes. Trends Biotechnol 27(3):148–153
Howard JB, Rees DC (1996) Structural basis of biological nitrogen fixation. Chem Rev 96:2965–2982
Hu Y, Ribbe MW (2013) Nitrogenase assembly. Biochim Biophys Acta 1827:1112–1122
Jamers A, Blust R, De Coen W (2009) Omics in algae: paving the way for a systems biological understanding of algal stress phenomena? Aquat Toxicol 92:114
Jones AK, Lamle SE, Pershad HR, Vincent KA, Albracht SPJ, Armstrong FA (2003) Enzyme electrokinetics: electrochemical studies of the anaerobic interconversions between active an inactive states of Allochromatium vinosum [NiFe] hydrogenase. J Am Chem Soc 125:8505–8514
Kallas T, Rebitre MC, Rippka R, Tandaeu de Marsa N (1983) The structural nif genes of the cyanobacterial Gloeothece sp. and Calothrix sp. share homology with those of Anabaena sp., but the Gloeothece genes have a different arrangement. J Bacteriol 155:427–431
Kalyanasundaram K, Graetzel M (2010) Artificial photosynthesis: biomimetic approaches to solar energy conversion and storage. Curr Opin Biotechnol 21:298–310
Kamp C, Silakov A, Winkler M, Reijerse EJ, Lubitz W, Happe T (2008) Isolation and first EPR characterization of the [FeFe]-hydrogenases from green algae. Biochim Biophys Acta 1777:410–416
Kessler E (1962) Hydrogenase und H2 Stoffwechsel bei algen vortr Gesamptgebiet. Bot NF 1:62–101
Kessler E (1974) Hydrogenase, photoreduction and anaerobic growth. In: Stewart WDP (ed) Algal physiology and biochemistry. Blackwell, Oxford, pp 456–473
Khetkorn W, Baebprasert W, Lindblad P, Incharoensakdi A (2012) Redirecting the electron flow towards the nitrogenase and bidirectional Hox-hydrogenase by using specific inhibitors results in enhanced H2 production in the cyanobacterium Anabaena siamensis TISTR 8012. Bioresour Technol 118:265–271
Kim DH, Kim MS (2011) Hydrogenases for biohydrogen production. Bioresour Technol 102:8423–8431
Kima JP, Kang CD, Park TY, Kim MS, Sim SJ (2006) Enhanced hydrogen production by controlling light intensity in sulphur deprived Chlamydomonas reinhardtii culture. Int J Hydrog Energy 31:1585–1590
King PW, Posewitz MC, Ghirardi ML, Seibert M (2006) Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system. J Bacteriol 188:2163–2172
Kojima E, Lin B (2004) Effect of partial shading on photoproduction of hydrogen by Chlorella. J Biosci Bioeng 97:317–321
Kosourov SN, Seibert M (2009) Hydrogen photoproduction by nutrient-deprived Chlamydomonas reinhardtii cells immobilized within thin alginate films under aerobic and anaerobic conditions. Biotechnol Bioeng 102:50–58
Kosourov S, Patrusheva E, Ghirardi ML, Seibert M, Tsygankov A (2007) A comparison of hydrogen photoproduction by sulfur-deprived Chlamydomonas reinhardtii under different growth conditions. J Biotechnol 128:776–787
Kosourov SN, Batyrova KA, Petushkova EP, Tsygankov AA, Maria LG, Seibert M (2012) Maximizing the hydrogen photoproduction yields in Chlamydomonas reinhardtii cultures: the effect of the H2 partial pressure. Int J Hydrog Energy 37:8850–8858
Kruse O, Rupprecht J, Bader KP, Thomas-Hall S, Schenk PM, Finazzi G, Hankamer B (2005) Improved photobiological H2 production in engineered green algal cells. J Biol Chem 280:34170–34177
Kufryk G (2013) Advances in utilizing cyanobacteria for hydrogen production. Adv Microbiol 3:60–68
Kützing FT (1849) Species algarum. FA Brockhaus, Leipzig
Lambertz C, Chernev P, Klingan K, Leidel N, Sigfridsson KGV, Happe T, Haumann M (2014) Electronic and molecular structures of the active-site H-cluster in [FeFe]-hydrogenase determined by site-selective X-ray spectroscopy and quantum chemical calculations. Chem Sci 5:1187–1203
Lamle SE, Halliwell LM, Armstrong FA, Albracht SP (2003) The electrochemical interconversions between the active and inactive states of a [NiFe]-hydrogenase; implications for the development of a bio-fuel cell. J Inorg Biochem 96:174
Laurinavichene T, Tolstygina I, Tsygankov A (2004) The effect of light intensity on hydrogen production by sulfur-deprived Chlamydomonas reinhardtii. J Biotechnol 114:143–151
Lee HS, Vermaas WFJ, Rittman BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28(5):262–271
Leite GB, Hallenbeck PC (2014) Engineered cyanobacteria: research and application in bioenergy. In: Gupta VK, Kubicek CP, Saddler J, Xu F, Tuohy MG (eds) Bioenergy research: advances and applications. Elsevier, Oxford. doi:10.1016/B978-0-444-59561-4.00022-X
Leon-Banares R, Gonza D, Galvan A, Fernandez E (2004) Transgenic microalgae as green cell-factories. Trends Biotechnol 22(1):45–52
Lindahl PA (2012) Metal–metal bonds in biology. J Inorg Chem 106:172–178
Lindblad P, Christensson K, Lindberg P, Fedorov A, Pinto F, Tsygankov A (2002) Photoproduction of H2 by wild type Anabaena PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture. Int J Hydrog Energy 27:1271–1281
Lopez D, Casero D, Cokus SJ, Merchant SS, Pellegrini M (2011) Algal functional annotation tool: a web based analysis suite to functionally interpret large gene lists using integrated annotation and expression data. BMC Bioinforma 12:282
Lubitz W, Ogata H, Rüdiger O, Reijerse E (2014) Hydrogenases. Chem Rev 114:4081–4148
Ludwig M, Schulz-Friedrich R, Appel J (2006) Occurrence of hydrogenases in cyanobacterial and anoxygenic photosynthetic bacteria: implications for phylogenetic origin of cyanobacterial and algal hydrogenases. J Mol Evol 63:758–768
Marr AC, Spencer DJE, Schroder M (2001) Structural mimics for the active site of [NiFe] hydrogenase. Coord Chem Rev 219–221:1055–1074
Martens R, Liese A (2004) Biotechnological applications of hydrogenases. Curr Opin Biotechnol 15:343–348
Masojidek J, Torzillo G, Koblizek M (2013) Photosynthesis in microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp 21–36
Mathews J, Wang G (2009) Metabolic pathway engineering for enhanced biohydrogen production. Int J Hydrog Energy 34:7404–7416
Matthew T, Zhou W, Rupprecht J, Lim L, Thomas-Hall SR, Doebbe A, Kruse O, Hankamer B, Marx UC, Smith SM, Schenk PM (2009) The metabolome of Chlamydomonas reinhardtii following induction of anaerobic H2 production by sulfur depletion. Curr Opin Biotechnol 284:23415–23425
May P, Christian JO, Kempa S, Walther D (2009) ChlamyCyc: an integrative systems biology database and web-portal for Chlamydomonas reinhardtii. BMC Genomics 10:209
Mayfield SP, Franklin SE (2005) Expression of human antibodies in eukaryotic micro-algae. Vaccine 23:1828–1832
McGlynn SE, Shepard EM, Winslow MA, Naumov AV, Duschene KS, Posewitz MC, Broderick WE (2008) FEMS Lett 582:2183–2187
Mckinlay JB, Harwood CS (2010) Photobiological production of hydrogen gas as a biofuel. Curr Opin Biotechnol 21:244–251
Melis A (2002) Green alga hydrogen production: progress, challenges and prospects. Int J Hydrog Energy 27:1217–1228
Melis A (2007) Photosynthetic H2 metabolism in Chlamydomonas reinhardtii (unicellular green algae). Planta 226:1075–1086
Melis A (2009) Solar energy conversion efficiencies in photosynthesis: minimizing the chlorophyll antenna to maximize efficiency. Plant Sci 177:272–280
Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748
Melis A, Zhang L, Forestier M, Ghirardi M, Seibert M (2000) Sustained photobiological hydrogen gas production upon reversible inactivation of oxygen evolution in the green alga Chlamydomonas reinhardtii. Plant Physiol 122:127–135
Merchant SS et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–250
Meuser JE, Boyd ES, Ananyey G, Karns D, Radakovits R, Narayana Murthy UM, GHirardi ML, Dismukes C, Peters JW, Posewitz MC (2011) Evolutionary significance of an algal gene encoding an [FeFe]-hydrogenase with F-domain homology and hydrogenase activity in Chlorella variabilis NC64A. Planta 234:829–843
Mevarech M, Rice D, Haselkorn R (1980) Nucleotide sequence of a cyanobacterial nifH gene coding for nitrogenase reductase. Proc Natl Acad Sci 77(11):6476–6480
Meyer TJ (1989) Chemical approaches to artificial photosynthesis. Acc Chem Res 22(163):170
Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084
Miyake J, Miyake M, Asada Y (1999) Biotechnological hydrogen production: research for efficient light energy conversion. J Biotechnol 70:89–101
Mulder DW, Shepard EM, Meuser JE, Joshi N, King PW, Posewitz MC, Broderick JB, Peters JB (2011) Insights into [FeFe]-hydrogenase structure, mechanism, and maturation. Structure 19:1038–1052
Mulligan ME, Haselkorn R (1989) Nitrogen fixation (nif) genes of the cyanobacterial Anabaena species strain PCC7120. J Biol Chem 264(32):19200–19207
Mus F, Cournac L, Cardettini V, Caruana A, Peltier G (2005) Inhibitor studies on non-photochemical PQ reduction and H2 photoproduction in Chlamydomonas reinhardtii. Biochim Biophys Acta 1708:322–332
Nguyen AV, Thomas-Hall SR, Malnoe A, Timmins M, Mussgnug JH, Rupprecht J, Kruse O, Hankamer O, Schenk PM (2008) Transcriptome for photobiological hydrogen production induced by sulfur deprivation in the green alga Chlamydomonas reinhardtii. Eukaryot Cell 7(11):1965–1979
Nguyen HM, Baudet M, Cuine S, Adriano JM, Barthe D, Billon E, Bruley C, Beisson F, Peltier G, Ferro M, Li-Beisson Y (2011) Proteomic profiling of oil bodies isolated from the unicellular green microalga Chlamydomonas reinhardtii: with focus on proteins involved in lipid metabolism. Proteomics 11:4266
Nicolet Y, Piras C, Legrand P, Hatchikian CE, Fontecilla-Camps JC (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23
Nicolet Y, Lemon BJ, Fontecilla-Camps JC, Peters JW (2000) A novel FeS cluster in Fe-only hydrogenases. TIBS 25:138–153
Nicolet Y, de Lacey AL, Vernede X, Fernandez VM, Hatchikian CE, Fontecilla-Camps JE (2001) Crystallographic and FTIR spectroscopic evidence of changes in Fe coordination upon reduction of the active site of the Fe-only-hydrogenase from Desulfovibrio desulfuricans. J Am Chem Soc 123:596–1601
Nicolet Y, Cavazza C, Fontecilla-Camps JC (2002) Fe only hydrogenases: structure, function and evolution. J Inorg Biochem 91:1–8
Nicolet Y, Fontecilla-Camps JC, Fontecava M (2010) Maturation of [FeFe]-hydrogenases: structures and mechanisms. Int J Hydrog Energy 35:10750–10760
Oh YK, Raj SM, Jung GY, Park S (2011) Current status of the metabolic engineering of microorganisms for biohydrogen production. Bioresour Technol 102:8357–8367
Okhi Y (2014) Synthetic analogous of the active sites of nitrogenase and [NiFe] hydrogenase. Bull Chem Soc Jpn 87(1):119
Oliveira Dal’Molin CG, Quek L-E, Palfreyman R, Nielsen L (2011) AlgaGEM–a genomescale metabolic reconstruction of algae based on the Chlamydomonas reinhardtii genome. BMC Genomics 12:S5
Oncel S (2013) Microalgae for a macro energy world. Renew Syst Energy Rev 26:241–264
Oncel SS (2015) Biohydrogen from microalgae, uniting energy, life, and green future. In: Kim SK (ed) Handbook of marine microalgae. Biotechnology Advances Academic Press, pp 159–196
Oncel S, Kose A (2014) Comparison of tubular and panel type photobioreactors for biohydrogen production utilizing Chlamydomonas reinhardtii considering mixing time and light intensity. Bioresour Technol 151:265–270
Oncel S, Sabankay M (2012) Microalgal biohydrogen production considering light energy and mixing time as the two key features for scale-up. Bioresour Technol 121:228–234
Oncel S, Kose A, Faraloni C, Imamoglu E, Elibol M, Torzillo G, Vardar Sukan F (2014) Biohydrogen production using mutant strains of Chlamydomonas reinhardtii: the effects of light intensity and illumination patterns. Biochem Eng J 92:47–52
Peters JW, Szilagyi RK (2006) Exploring new frontiers of nitrogenase structure and mechanism. Curr Opin Chem Biol 10:101–108
Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858
Peters JW, Szilagyi RK, Naumov A, Douglas T (2006) A radical solution for the biosynthesis of the H-cluster of hydrogenase. FEBS Lett 580:363–367
Pierik AJ, Hulstein M, Hagen WR, Albracht SPJ (1998) A low-spin iron with CN and CO as intrinsic ligands forms the core of the active site in [Fe]-hydrogenases. Eur J Biochem 258:572–578
Polle JEW, Kanakagiri S, Jin ES, Masuda T, Melis A (2002) Truncated chlorophyll antenna size of the photosystems – a practical method to improve microalgal productivity and hydrogen production in mass culture. Int J Hydrog Energy 27:1257–1264
Posewitz MC, King PW, Smolinski SL, Zhang L, Seibert M, Ghirardi ML (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720
Postgate JR, Eady RR (1988) The evolution of biological nitrogen fixation. In: Bothe H, de Bruijn FJ, Newton WE (eds) Nitrogen fixation: hundred years after. Gustav Fischer, Stuttgart, pp 31–40
Prince RC, Kheshgi HD (2005) The photobiological production of hydrogen: potential efficiency and effectiveness as a renewable fuel. Crit Rev Microbiol 31:19–31
Rees DC, Howard JB (2000) Nitrogenase: standing at the crossroads. Curr Opin Chem Biol 4:559–566
Rice D, Mazur BJ, Haselkorn R (1982) Isolation and physical mapping of nitrogen fixation genes from the cyanobacterium Anabaena 7120. J Biol Chem 257(21):13157–13163
Rismandi Yazdi H, Haznedaroglu BZ, Bibby K, Peccia J (2011) Transcriptome sequencing and annotation of the microalgae Dunaliella tertiolecta: pathway description and gene discovery for production of next-generation biofuels. BMC Genomics 12:148
Rolland N, Atteia A, Decottignies P, Garin J, Hippler M, Kreimer G, Lemaire SD, Mittag M, Wagner V (2009) Chlamydomonas proteomics. Curr Opin Microbiol 12(3):285–291
Roseboom W, de Lacey AL, Fernandez WM, Hatchikian CE, Albracht SPJ (2006) The active site of the [FeFe]-hydrogenase from Desulfovibrio desulfuricans. II. Redox properties, light sensitivity and CO-ligand exchange as observed by infrared spectroscopy. J Biol Inorg Chem 11:102–118
Rosenberg JN, Oyler GA, Wilkinson L, Betenbaugh MJ (2008) A green light for engineered algae: redirecting metabolism to fuel a biotechnology revolution. Curr Opin Biotechnol 19:430–436
Rubach JK, Brazzolotto X, Gaillard J, Fontecave M (2005) Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579:5055–5060
Rubio LM, Ludden PW (2005) Maturation of nitrogenase: a biochemical puzzle. J Bacteriol 187(2):405–414
Rupprecht J (2009) From system biology to fuel-Chlamydomonas reinhardtii as a model for a systems biology approach to improve biohydrogen production. J Biotechnol 142:10–20
Sakurai H, Masukawa H, Kitashima M, Inoue K (2013) Photobiological hydrogen production: bioenergetics and challenges for its practical application. J Photochem Photobiol C 17:1–25
Saleem M, Chakrabarti M, Raman AAA, Hasan DB, Dauad WMAW, Mustafa A (2012) Hydrogen production by Chlamydomonas reinhardtii in a two-stage process with and without illumination at alkaline pH. Int J Hydrog Energy 37:4930–4934
Schawarz G, Mendel RR, Ribbe MW (2009) Molybdenum cofactors, enzymes and pathways. Nature 460(13). doi: 10.1038/nature08302
Schmitter JM, Jacquot JP, de Lamotte-Guery F, Beauvallet C, Dutka S, Gadal P et al (1998) Purification, properties and complete amino acid sequence of the ferredoxin from a green alga, Chlamydomonas reinhardtii. Eur J Biochem 172:405–412
Scoma A, Krawietz D, Faraloni C, Giannelli L, Happe T, Torzillo G (2012) Sustained H2 production in a Chlamydomonas reinhardtii D1 protein mutant. J Biotechnol 157:613–619
Seefeldt LC, Hoffman BM, Dean DR (2012) Electron transfer in nitrogenase catalysis. Curr Opin Chem Biol 16:19–25
Shafaat HS, Rüdriger O, Ogata H, Lubitz W (2013) [NiFe] hydrogenases: a common active site for hydrogen metabolism under diverse conditions. Biochim Biophys Acta 1827:986–1002
Shepard EM, Boyd ES, Broderick JB, Peters JW (2011) Biosynthesis of complex iron-sulfur enzymes. Curr Opin Chem Biol 15:319–327
Skjanes K, Pinto FL, Lindblad P (2010) Evidence for transcription of three genes with characteristics of hydrogenases in the green alga Chlamydomonas noctigama. Int J Hydrog Energy 35:1074–1088
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial applications of microalgae. J Biosci Bioeng 101:87–96
Srirangan K, Pyne ME, Chou CP (2011) Biochemical and genetic engineering strategies to enhance hydrogen production in photosynthetic algae and cyanobacterial. Bioresour Technol 102:8589–8604
Stephenson M, Stickland SH (1931) Hydrogenase: a bacterial enzyme activating molecular hydrogen. I. The properties of hydrogenases. Biochem J 25:205–214
Sun L, Akermark B, Ott S (2005) Iron hydrogenase active site mimics in supramolecular systems aiming for light-driven hydrogen production. Coord Chem Rev 249:1653–1663
Surzycki R, Cournac L, Peltier G, Rochaix JD (2007) Potential for hydrogen production with inducible chloroplast gene expression in Chlamydomonas. Proc Natl Acad Sci U S A 104:17548–17553
Switzer L (1981) Spirulina: the whole food revolution. Proteus Corporation Banta Books, Toronto
Sybirna K, Ezanno P, Baffert C, Leger C, Bottin H (2013) Arginine171 of Chlamydomonas reinhardtii [FeeFe] hydrogenase HydA1 plays a crucial role in electron transfer to its catalytic center. Int J Hydrog Energy 38:2998–3002
Tamagnini P, Axelsson R, Lindberg P, Oxelfelt F, Wünschiers R, Lindblad P (2002) Hydrogenases and hydrogen metabolism of cyanobacteria. Microbiol Mol Biol Rev 66(1):1–20
Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenase: diversity, regulation and applications. FEMS Microbiol Rev 31(6):692–720
Taylor B, Lee C, Bunt J (1973) Nitrogen-fixation associated with the marine blue-green alga, Trichodesmium, as measured by the acetylene-reduction technique. Arch Mikrobiol 88:205–212
Thompson AW, Zehr JP (2013) Cellular interactions: lessons from the nitrogen fixing cyanobacteria. J Phycol 49:1024–1035
Torzillo G, Seibert M (2013) Hydrogen production by microalgae. In: Richmond A, Hu Q (eds) Handbook of microalgal culture: applied phycology and biotechnology, 2nd edn. Wiley, Oxford, pp 417–444
Torzillo G, Scoma A, Faraloni C, Gianelli L (2014) Advances in the biotechnology of hydrogen production with the microalga Chlamydomonas reinhardtii. Crit Rev Biotechnol:1–12. doi: 10.3109/07388551.2014.900734
Tóth SZ, Schansker G, Garab G, Strasser RJ (2007) Photosynthetic electron transport activity in heat-treated barley leaves, the role of internal alternative electron donors to photosystem II. BBA Bioenerg 1767:295–305
Tsygankov AA (2007) Nitrogen fixing cyanobacteria: a review. Appl Biochem Microbiol 43(3):250–259
Tsygankov A, Kosourov S, Seibert M, Ghirardi ML (2002) Hydrogen photoproduction under continuous illumination by sulfur deprived, synchronous Chlamydomonas reinhardtii cultures. Int J Hydrog Energy 27:1239–1244
Vignais PN, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501
Volbeda SA, Fontecilla-Camps JC (2005) Structure–function relationships of nickel–iron sites in hydrogenase and a comparison with the active sites of other nickel–iron enzymes. Coord Chem Rev 249:1609–1619
Volbeda A, Charon MH, Piras C, Hatchikian EC, Frey M, Fontecilla-Camps JC (1995) Cystal structure of [NiFe] hydrogenase. Nature 373:580–587
Walker TL, Collet C, Purton S (2005) Algal transgenics in the genomic era. J Phycol 41:1077–1093
Weckwerth W (2011) Green systems biology – from single genomes, proteomes and metabolomes to ecosystems research and biotechnology. J Proteomics 875:284–305
Wilmotte A, Herdman M (2001) In: Boone DR, Castenholz RW (eds) Phylogenetic relationships among the cyanobacteria based on 16S rRNA sequences, Bergey’s manual of systematic bacteriology, 2nd edn. Springer-Verlag, New York, pp 487–493
Winkler M, Heil B, Happe T (2002a) Isolation and molecular characterization of the [Fe]-hydrogenase from the unicellular green alga Chlorella fusca. Biochim Biophys Acta 1576:330–334
Winkler M, Hemscheimer A, Gotor C, Melis A, Happe T (2002b) [Fe]-hydrogenases in green algae: photo-fermentation and hydrogen evolution under sulfur deprivation. Int J Hydrog Energy 27(11–12):1431–1439
Winkler M, Kuhlgert S, Hippler M, Happe T (2009) Characterization of the key step for light-driven hydrogen evolution in green algae. J Biol Chem 284(52):36620–36627
Winkler M, Esselborn J, Happe T (2013) Molecular basis of [FeFe]-hydrogenase function: an insight into the complex interplay between protein and catalytic cofactor. Bioch Biophys Acta 1827:974–985
Wykoff DD, Davies JP, Melis A, Grossman AR (1998) The regulation of photosynthetic electron transport during nutrient deprivation in Chlamydomonas reinhardtii. Plant Physiol 117:129–139
Yacoby I, Tegler LT, Pochekailov S, Zhang S, King PW (2012) Optimized expression and purification for high-activity preparations of algal [FeFe]-hydrogenase. PLoS One 7:35886
Young JPW (1992) Phylogenetic classification of nitrogenfixing organisms. In: Stacey G, Evans HJ, Burris RH (eds) Biological nitrogen fixation. Chapman & Hall, New York, pp 43–86
Zehr JP, Jenkins BD, Short SM, Steward GF (2003) Nitrogenase gene diversity and microbial community structure: a cross-system comparison. Environ Microbiol 7:539–554
Zhang L, Happe T, Melis A (2002) Biochemical and morphological characterization of sulfur-deprived and H2-producing Chlamydomonas reinhardtii (green alga). Planta 214:552–561
Zhang L, He M, Liu J (2014) The enhancement mechanism of hydrogen photoproduction in Chlorella protothecoides under nitrogen limitation and sulfur deprivation. Int J Hydrog Energy 39:8969–8976
Zhao Y, Bian SM, Zhou HN, Huang JF (2006) Diversity of nitrogenase systems in diazotrophs. Plant Biol 48(7):745–755
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Kose, A., Oncel, S.S. (2017). Biohydrogen Production from Microalgae: An Enzyme Perspective. In: Singh, A., Rathore, D. (eds) Biohydrogen Production: Sustainability of Current Technology and Future Perspective. Springer, New Delhi. https://doi.org/10.1007/978-81-322-3577-4_9
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