Summary
The use of microalgae for production of hydrogen gas from water photolysis has been studied for many years, but its commercialization is still limited by multiple challenges. Most of the barriers to commercialization are attributed to the existence of biological regulatory mechanisms that, under anaerobic conditions, quench the absorbed light energy, down-regulate linear electron transfer, inactivate the H2-producing enzyme, and compete for electrons with the hydrogenase. Consequently, the conversion efficiency of absorbed photons into H2 is significantly lower than its estimated potential of 12–13 %. However, extensive research continues towards addressing these barriers by either trying to understand and circumvent intracellular regulatory mechanisms at the enzyme and metabolic level or by developing biological systems that achieve prolonged H2 production albeit under lower than 12–13 % solar conversion efficiency. This chapter describes the metabolic pathways involved in biological H2 photoproduction from water photolysis, the attributes of the two hydrogenases, [FeFe] and [NiFe], that catalyze biological H2 production, and highlights research related to addressing the barriers described above. These highlights include: (a) recent advances in improving our understanding of the O2 inactivation mechanism in different classes of hydrogenases; (b) progress made in preventing competitive pathways from diverting electrons from H2 photoproduction; and (c) new developments in bypassing the non-dissipated proton gradient from down-regulating photosynthetic electron transfer. As an example of a major success story, we mention the generation of truncated-antenna mutants in Chlamydomonas and Synechocystis that address the inherent low-light saturation of photosynthesis. In addition, we highlight the rationale and progress towards coupling biological hydrogenases to non-biological, photochemical charge-separation as a means to bypass the barriers of photobiological systems.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
Abbreviations
- ATP:
-
– Adenosine triphosphate;
- CCCP:
-
– Carbonyl cyanide m-chloro phenyl hydrazone;
- CEF:
-
– Cyclic electron flow;
- CRR1 –:
-
Copper response regulator 1;
- DCIP:
-
– Dichlorophenol indophenol;
- DCMU:
-
– (3-(3,4-dichlorophenyl)-1,1-dimethylurea);
- DHG:
-
– Dehydroglycine;
- EPR:
-
– Electron paramagnetic resonance;
- ET:
-
– Electron transfer;
- ETR:
-
– Electron transport rate;
- FCCP:
-
– Carbonylcyanide p-fluoromethoxyphenylhydrazone;
- FDX:
-
– Ferredoxin;
- FNR:
-
– Ferredoxin/NADP oxido-reductase;
- FTIR:
-
– Fourier transform infrared spectroscopy;
- ISC:
-
– Iron-sulfur cluster;
- LEF:
-
– Linear electron flow;
- LHC:
-
– Light-harvesting complex;
- MBH:
-
– Membrane-bound hydrogenase;
- MWNT:
-
– Multi-walled carbon nanotubes;
- NAD(P):
-
– Nicotinamide adenine (phosphate) dinucleotide;
- NPQ:
-
– Non-photochemical quenching;
- OEC:
-
– Oxygen-evolving complex;
- OCP:
-
– Orange carotenoid protein;
- PFR:
-
– Pyruvate/ferredoxin reductase;
- PQ:
-
– Plastoquinone;
- PSI:
-
– Photosystem I;
- PSII:
-
– Photosystem II;
- PTOX:
-
– Plastoquinone oxidase;
- SAM –:
-
S-adenosyl methionine;
- SAXS:
-
– Small angle X-ray scattering;
- SWNT:
-
– Single walled carbon nanotubes;
- WT:
-
– Wild-type
References
Adams MWW (1990) The structure and mechanism of iron-hydrogenases. Biochim Biophys Acta 1020:115–145
Adams MWW, Mortenson LE, Chen JS (1980) Hydrogenase. Biochim Biophys Acta 594:105–176
Agapakis CM, Ducat DC, Boyle PM, Wintermute EH, Way JC, Silver PA (2010) Insulation of a synthetic hydrogen metabolism circuit in bacteria. J Biol Eng 4:3
Ai X, Xu Q, Jones M, Song Q, Ding SY, Ellingson RJ, Himmel M, Rumbles G (2007) Photophysics of (CdSe) ZnS Colloidal quantum dots in an aqueous environment stabilized with amino acids and genetically-modified proteins. Photochem Photobiol Sci 6:1027–1033
Akhtar MK, Jones PR (2008) Engineering of a synthetic hydF-hydE-hydG-hydA operon for biohydrogen production. Anal Biochem 373:170–172
Akhtar MK, Jones PR (2009) Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3). Metab Eng 11:139–147
Allakhverdiev SI, Kreslavski VD, Thavasi V, Zharmukhamedov SK, Klimov VV, Nagata T, Nishihara H, Ramakrishna S (2009) Hydrogen photoproduction by use of photosynthetic organisms and biomimetic systems. Photochem Photobiol Sci 8:148–156
Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335
Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19
Alonso-Lomillo MA, Rudiger O, Maroto-Valiente A, Velez M, Rodriguez-Ramos I, Munoz FJ, Fernandez VM, De Lacey AL (2007) Hydrogenase-coated carbon nanotubes for efficient H2 oxidation. Nano Lett 7:1603–1608
Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106:47–56
Amirav L, Alivisatos AP (2010) Photocatalytic hydrogen production with tunable nanorod heterostructures. J Phys Chem Lett 1:1051–1054
Antal TK, Oliveira P, Lindblad P (2006) The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrog Energy 31:1439–1444
Appel J, Schulz R (1996) Sequence analysis of an operon of a NAD(P)-reducing nickel hydrogenase from the cyanobacterium Synechocystis sp. PCC 6803 gives additional evidence for direct coupling of the enzyme to NAD(P)H-dehydrogenase (complex I). Biochim Biophys Acta 1298:141–147
Appel J, Phunpruch S, Steinmuller K, Schulz R (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173:333–338
Armstrong FA, Hirst J (2011) Reversibility and efficiency in electrocatalytic energy conversion and lessons from enzymes. Proc Natl Acad Sci U S A 108:14049–14054
Armstrong FA, Heering HA, Hirst J (1997) Reactions of complex metalloproteins studied by protein-film voltammetry. Chem Soc Rev 26:169–179
Armstrong FA, Belsey NA, Cracknell JA, Goldet G, Parkin A, Reisner E, Vincent KA, Wait AF (2009) Dynamic electrochemical investigations of hydrogen oxidation and production by enzymes and implications for future technology. Chem Soc Rev 38:36–51
Asada Y, Koike Y, Schnackenberg J, Miyake M, Uemura I, Miyake J (2000) Heterologous expression of clostridial hydrogenase in the cyanobacterium Synechococcus PCC7942. Biochim Biophys Acta 1490:269–278
Axelsson R, Lindblad P (2002) Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. Appl Environ Microbiol 68:444–447
Badia A, Lennox RB, Reven L (2000) A dynamic view of self-assembled monolayers. Acc Chem Res 33:475–481
Badura A, Guschin D, Esper B, Kothe T, Neugebauer S, Schuhmann W, Rögner M (2008) Photo-induced electron transfer between photosystem II via cross-linked redox hydrogels. Electroanalysis 20:1043–1047
Bae B, Kho BK, Lim TH, Oh IH, Hong SA, Ha HY (2006) Performance evaluation of passive DMFC single cells. J Power Sources 158:1256–1261
Bae S, Shim E, Yoon J, Joo H (2008) Photoanodic and cathodic role of anodized tubular titania in light-sensitized enzymatic hydrogen production. J Power Sources 185:439–444
Baebprasert W, Lindblad P, Incharoensakdi A (2010) Response of H2 production and Hox-hydrogenase activity to external factors in the unicellular cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydrog Energy 35:6611–6616
Baffert C, Bertini L, Lautier T, Greco C, Sybirna K, Ezanno P, Etienne E, Soucaille P, Bertrand P, Bottin H, Meynial-Salles I, De Gioia L, Leger C (2011) CO disrupts the reduced H-Cluster of FeFe hydrogenase. A combined DFT and protein film voltammetry study. J Am Chem Soc 133:2096–2099
Baltazar CSA, Marques MC, Soares CM, DeLacey AM, Pereira IAC, Matias PM (2011) Nickel-iron-selenium hydrogenases – an overview. Eur J Inorg Chem 2011:948–962
Bandyopadhyay A, Stockel J, Min H, Sherman LA, Pakrasi HB (2010) High rates of photobiological H2 production by a cyanobacterium under aerobic conditions. Nat Commun 1:139
Barstow B, Agapakis CM, Boyle PM, Grandl G, Silver PA, Wintermute EH (2011) A synthetic system links [FeFe]-hydrogenases to essential E. coli sulfur metabolism. J Biol Eng 5:7
Battchikova N, Wei L, Du L, Bersanini L, Aro EM, Ma W (2011) Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH: plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. J Biol Chem 286:36992–37001
Benemann J (1989) The future of microalgal biotechnology. In: Cresswell RC, Rees TAV, Shah N (eds) Algal and cyanobacterial biotechnology. Longman Scientific and Technical, Harlow, pp 317–337
Bennett B, Lemon BJ, Peters JW (2000) Reversible carbon monoxide binding and inhibition at the active site of the Fe-only hydrogenase. Biochemistry 39:7455–7460
Bernat G, Waschewski N, Rogner M (2009) Towards efficient hydrogen production: the impact of antenna size and external factors on electron transport dynamics in Synechocystis PCC 6803. Photosynth Res 99:205–216
Berto P, D’Adamo S, Bergantino E, Vallese F, Giacometti GM, Costantini P (2011) The cyanobacterium Synechocystis sp. PCC 6803 is able to express an active [FeFe] -hydrogenase without additional maturation proteins. Biochem Biophys Res Commun 405:678–683
Blackburn JL, Svedruzic D, McDonald TJ, Kim YH, King PW, Heben MJ (2008) Raman spectroscopy of charge transfer interactions between single wall carbon nanotubes and [FeFe]-hydrogenase. Dalton Trans 40:5454–5461
Blankenship RE, Tiede DM, Barber J, Brudvig GW, Fleming G, Ghirardi M, Gunner MR, Junge W, Kramer DM, Melis A, Moore TA, Moser CC, Nocera DG, Nozik AJ, Ort DR, Parson WW, Prince RC, Sayre RT (2011) Comparing photosynthetic and photovoltaic efficiencies and recognizing the potential for improvement. Science 332:805–809
Blokesch M, Bock A (2002) Maturation of [NiFe]-hydrogenases in Escherichia coli: the HypC cycle. J Mol Biol 324:287–296
Bock A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71
Boison G, Schmitz O, Schmitz B, Bothe H (1998) Unusual gene arrangement of the bidirectional hydrogenase and functional analysis of its diaphorase subunit HoxU in respiration of the unicellular cyanobacterium Anacystis nidulans. Curr Microbiol 36:253–258
Boison G, Bothe H, Hansel A, Lindblad P (1999) Evidence against a common use of the diaphorase subunits by the bidirectional hydrogenase and by the respiratory complex I in cyanobacteria. FEMS Microbiol Lett 174:159–165
Boison G, Bothe H, Schmitz O (2000) Transcriptional analysis of hydrogenase genes in the cyanobacteria Anacystis nidulans and Anabaena variabilis monitored by RT-PCR. Curr Microbiol 40:315–321
Bolton JR, Strickler SJ, Connolly JS (1985) Limiting and realizable efficiencies of solar photolysis of water. Nature 316:495–500
Bothe H, Schmitz O, Yates MG, Newton WE (2011) Nitrogenases and hydrogenases in cyanobacteria. In: Peschek GA, Obinger C, Renger G (eds) Bioenergetic processes of cyanobacteria. Springer Science Publishing, pp 137–157
Brand JJ, Wright JN, Lien S (1989) Hydrogen-production by eukaryotic algae. Biotechnol Bioeng 33:1482–1488
Brazzolotto X, Rubach JK, Gaillard J, Gambarelli S, Atta M, Fontecave M (2006) The [Fe-Fe]-hydrogenase maturation protein HydF from Thermotoga maritima is a GTPase with an iron-sulfur cluster. J Biol Chem 281:769–774
Brown KA, Dayal S, Xin A, Rumbles G, King PW (2010) Controlled assembly of hydrogenase-CdTe nanocrystal hybrids for solar hydrogen production. J Am Chem Soc 132:9672–9680
Brown KA, Wilker MB, Boehm M, Dukovic G, King PW (2012) Characterization of photochemical processes for H2 production by CdS nanorod- [FeFe]-hydrogenase complexes. J Am Chem Soc 134:5627–5636
Bruce BD (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10:440–447
Buhrke T, Bleijlevens B, Albracht SPJ, Friedrich B (2001) Involvement of hyp gene products in maturation of the H2-sensing [NiFe] hydrogenase of Ralstonia eutropha. J Bacteriol 183:7087–7093
Burgdorf T, Lenz O, Buhrke T, van der Linden E, Jones AK, Albracht SP, Friedrich B (2005) [NiFe]-hydrogenases of Ralstonia eutropha H16: modular enzymes for oxygen-tolerant biological hydrogen oxidation. J Mol Microbiol Biotechnol 10:181–196
Cardol P, Alric J, Girard-Bascou J, Franck F, Wollman FA, Finazzi G (2009) Impaired respiration discloses the physiological significance of state transitions in Chlamydomonas. Proc Natl Acad Sci U S A 106:15979–15984
Carrieri D, Wawrousek K, Eckert C, Yu J, Maness PC (2011) The role of the bidirectional hydrogenase in cyanobacteria. Bioresour Technol 102:8368–8377
Cendron L, Berto P, D’Adamo S, Vallese F, Govoni C, Posewitz MC, Giacometti GM, Costantini P, Zanotti G (2011) Crystal structure of HydF scaffold protein provides insights into [FeFe]-hydrogenase maturation. J Biol Chem 286:43944–43950
Chang CH, King PW, Ghirardi ML, Kim K (2007) Atomic resolution modeling of the ferredoxin:[FeFe] hydrogenase complex from Chlamydomonas reinhardtii. Biophys J 93:3034–3045
Chen XJ, Schnell DJ (1999) Protein import into chloroplasts. Trends Cell Biol 9:222–227
Chen Z, Lemon BJ, Huang S, Swartz DJ, Peters JW, Bagley KA (2002) Infrared studies of the CO-inhibited form of the Fe-only hydrogenase from Clostridium pasteurianum I: examination of its light sensitivity at cryogenic temperatures. Biochemistry 41:2036–2043
Chen XB, Shen SH, Guo LJ, Mao SS (2010) Semiconductor-based photocatalytic hydrogen generation. Chem Rev 110:6503–6570
Chung KCC, Zamble DB (2011) Protein interactions and localization of the Escherichia coli accessory protein HypA during nickel insertion to [NiFe] hydrogenase. J Biol Chem 286:43081–43090
Cohen J, Kim K, King P, Seibert M, Schulten K (2005a) Finding gas diffusion pathways in proteins: application to O2 and H2 transport in CpI [FeFe]-hydrogenase and the role of packing defects. Structure 13:1321–1329
Cohen J, Kim K, Posewitz M, Ghirardi ML, Schulten K, Seibert M, King P (2005b) Molecular dynamics and experimental investigation of H2 and O2 diffusion in [Fe]-hydrogenase. Biochem Soc Trans 33:80–82
Cornish AJ, Gartner K, Yang H, Peters JW, Hegg EL (2011) Mechanism of proton transfer in [FeFe]-hydrogenase from Clostridium pasteurianum. J Biol Chem 286:38341–38347
Cournac L, Mus F, Bernard L, Guedeney G, Vignais P, Peltier G (2002) Limiting steps of hydrogen production in Chlamydomonas reinhardtii and Synechocystis PCC 6803 as analysed by light-induced gas exchange transients. Int J Hydrog Energy 27:1229–1237
Cournac L, Guedeney G, Peltier G, Vignais PM (2004) Sustained photoevolution of molecular hydrogen in a mutant of Synechocystis sp. strain PCC 6803 deficient in the type I NADPH-dehydrogenase complex. J Bacteriol 186:1737–1746
Cracknell JA, Vincent KA, Armstrong FA (2008) Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. Chem Rev 108:2439–2461
Cuendet P, Rao KK, Grätzel M, Hall DO (1986) Light induced H2 evolution in a hydrogenase-TiO2 particle system by direct electron transfer or via rhodium complexes. Biochimie 68:217–221
Czech I, Silakov A, Lubitz W, Happe T (2010) The [FeFe]-hydrogenase maturase HydF from Clostridium acetobutylicum contains a CO and CN- ligated iron cofactor. FEBS Lett 584:638–642
Czech I, Stripp S, Sanganas O, Leidel N, Happe T, Haumann M (2011) The [FeFe]-hydrogenase maturation protein HydF contains a H-cluster like [4Fe4S]-2Fe site. FEBS Lett 585:225–230
DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schunemann D, Finazzi G, Joliot P, Barbato R, Leister D (2008) A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in Arabidopsis. Cell 132:273–285
Desplats C, Mus F, Cuine S, Billon E, Cournac L, Peltier G (2009) Characterization of Nda2, a plastoquinone-reducing type II NAD(P)H dehydrogenase in Chlamydomonas chloroplasts. J Biol Chem 284:4148–4157
Devine E, Holmqvist M, Stensjo K, Lindblad P (2009) Diversity and transcription of proteases involved in the maturation of hydrogenases in Nostoc punctiforme ATCC 29133 and Nostoc sp. strain PCC 7120. BMC Microbiol 9:53
Driesener RC, Challand MR, McGlynn SE, Shepard EM, Boyd ES, Broderick JB, Peters JW, Roach PL (2010) [FeFe]-hydrogenase cyanide ligands derived from S-adenosylmethionine-dependent cleavage of tyrosine. Angew Chem Int Ed Engl 49:1687–1690
Ducat DC, Sachdeva G, Silver PA (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci U S A 108:3941–3946
Dukovic G, Merkle MG, Nelson JH, Hughes SM, Alivisatos AP (2008) Photodeposition of Pt on colloidal CdS and CdSe/CdS semiconductor nanostructures. Adv Mater 20:4306–4311
Dutheil J, Saenkham P, Sakr S, Leplat C, Ortega-Ramos M, Bottin H, Cournac L, Cassier-Chauvat C, Chauvat F (2012) Advances in the regulation of hydrogen production in Synechocystis PCC6803: the AbrB2 auto-repressor (sll0822), expressed from an atypical promoter, represses the hydrogenase operon. J Bacteriol 194:5423–5433
Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515
Eckert C, Boehm M, Carrieri D, Yu J, Dubini A, Nixon PJ, Maness PC (2012a) Genetic analysis of the Hox hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 reveals subunit roles in association, assembly, maturation, and function. J Biol Chem 287:43502–43515
Eckert C, Dubini A, Yu J, King P, Ghirardi ML, Seibert M, Maness PC (2012b) Hydrogenase genes and enzymes involved in solar hydrogen production. In: Levin DB, Azbar N (eds) State of the art and progress in production of biohydrogen, vol 1. Bentham Science Publisher, Sarjah, UAE, pp 8–24
Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816
English CM, Eckert CA, Brown KA, Seibert M, King PW (2009) Recombinant and in vitro expression systems for hydrogenases: new frontiers in basic and applied studies for biological and synthetic H2 production. Dalton Trans 45:9970–9978
Erbes DL, King D, Gibbs M (1978) Effect of carbon monoxide and oxygen on hydrogen activation by hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 61:23
Erbes DL, King D, Gibbs M (1979) Inactivation of hydrogenase in cell-free extracts and whole cells of Chlamydomonas reinhardtii by oxygen. Plant Physiol 63:1138–1142
Erdem OF, Schwartz L, Stein M, Silakov A, Kaur-Ghumaan S, Huang P, Ott S, Reijerse EJ, Lubitz W (2011) A model of the [FeFe] hydrogenase active site with a biologically relevant azadithiolate bridge: a spectroscopic and theoretical investigation. Angew Chem Int Ed Engl 50:1439–1443
Eroglu E, Melis A (2011) Photobiological hydrogen production: recent advances and state of the art. Bioresour Technol 102:8403–8413
Esper B, Badura A, Rogner M (2006) Photosynthesis as a power supply for biohydrogen production. Trends Plant Sci 11:543–549
Ferreira D, Leitao E, Sjoholm J, Oliveira P, Lindblad P, Moradas-Ferreira P, Tamagnini P (2007) Transcription and regulation of the hydrogenase(s) accessory genes, hypFCDEAB, in the cyanobacterium Lyngbya majuscula CCAP 1446/4. Arch Microbiol 188:609–617
Finazzi G, Furia A, Barbagallo RP, Forti G (1999) State transitions, cyclic and linear electron transport and photophosphorylation in Chlamydomonas reinhardtii. Biochim Biophys Acta 1413:117–129
Fischer N, Setif P, Rochaix JD (1999) Site-directed mutagenesis of the PsaC subunit of photosystem I. F(b) is the cluster interacting with soluble ferredoxin. J Biol Chem 274:23333–23340
Fitzgerald MP, Rogers LJ, Rao KK, Hall DO (1980) Efficiency of ferredoxins and flavodoxins as mediators in systems for hydrogen evolution. Biochem J 192:665–672
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
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 Hydrog Energy 27:1421–1430
Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303
Forestier M, King P, Zhang L, Posewitz M, Schwarzer S, Happe T, Ghirardi ML, Seibert M (2003) Expression of two [Fe]-hydrogenases in Chlamydomonas reinhardtii under anaerobic conditions. Eur J Biochem 270:2750–2758
Forti G, Furia A, Bombelli P, Finazzi G (2003) In vivo changes of the oxidation-reduction state of NADP and of the ATP/ADP cellular ratio linked to the photosynthetic activity in Chlamydomonas reinhardtii. Plant Physiol 132:1464–1474
Fouchard S, Hemschemeier A, Caruana A, Pruvost J, Legrand J, Happe T, Peltier G, Cournac L (2005) Autotrophic and mixotrophic hydrogen photoproduction in sulfur-deprived Chlamydomonas cells. Appl Environ Microbiol 71:6199–6205
Fritsch J, Loscher S, Sanganas O, Siebert E, Zebger I, Stein M, Ludwig M, De Lacey AL, Dau H, Friedrich B, Lenz O, Haumann M (2011) [NiFe] and [FeS] cofactors in the membrane-bound hydrogenase of Ralstonia eutropha investigated by X-ray absorption spectroscopy: insights into O2-tolerant H2 cleavage. Biochemistry 50:5858–5869
Galvan IF, Volbeda A, Fontecilla-Camps JC, Field MJ (2008) A QM/MM study of proton transport pathways in a [NiFe] hydrogenase. Proteins Struct Funct Bioinform 73:195–203
Gaponik N, Talapin DV, Rogach AL, Hoppe K, Shevchenko EV, Kornowski A, Eychmuller A, Weller H (2002) Thiol-capping of CdTe nanocrystals: an alternative to organometallic synthetic routes. J Phys Chem B 106:7177–7185
Garcia-Sanchez MI, Gotor C, Jacquot JP, Stein M, Suzuki A, Vega JM (1997) Critical residues of Chlamydomonas reinhardtii ferredoxin for interaction with nitrite reductase and glutamate synthase revealed by site-directed mutagenesis. Eur J Biochem 250:364–368
Germer F, Zebger I, Saggu M, Lendzian F, Schulz R, Appel J (2009) Overexpression, isolation, and spectroscopic characterization of the bidirectional [NiFe] hydrogenase from Synechocystis sp. PCC 6803. J Biol Chem 284:36462–36472
Gfeller RP, Gibbs M (1984) Fermentative metabolism of Chlamydomonas reinhardtii: I. analysis of fermentative products from starch in dark and light. Plant Physiol 75:212–218
Ghirardi ML, Togasaki R, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63–65:141–151
Ghirardi ML, Posewitz MC, Maness PC, Dubini A, Yu J, Seibert M (2007) Hydrogenases and hydrogen photoproduction in oxygenic photosynthetic organisms. Annu Rev Plant Biol 58:71–91
Ghirardi ML, Dubini A, Yu J, Maness PC (2009) Photobiological hydrogen-producing systems. Chem Soc Rev 38:52–61
Ghysels B, Franck F (2010) Hydrogen photo-evolution upon S deprivation stepwise: an illustration of microalgal photosynthetic and metabolic flexibility and a step stone for future biotechnological methods of renewable H2 production. Photosynth Res 106:145–154
Gillez-Gonzalez MA, Gonzalez G, Perutz MF, Kiger L, Marden MC, Poyart C (1994) Heme-based sensors, exemplified by the kinase fixL, are a new class of heme protein with distinctive ligand binding and autoxidation. Biochemistry 33:8067–8073
Godman JE, Molnar A, Baulcombe DC, Balk 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
Goldet G, Brandmayr C, Stripp ST, Happe T, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009) Electrochemical kinetic investigations of the reactions of [FeFe]-hydrogenases with carbon monoxide and oxygen: comparing the importance of gas tunnels and active-site electronic/redox effects. J Am Chem Soc 131:14979–14989
Greene BL, Joseph CA, Maroney MJ, Dyer RB (2012) Direct evidence of active-site reduction and photodriven catalysis in sensitized hydrogenase assemblies. J Am Chem Soc 134:11108–11111
Gubili J, Borthakur D (1998) Organization of the hupDEAB genes within the hydrogenase gene cluster of Anabaena sp. strain PCC7120. J Appl Phycol 10:163–167
Guldi DM, Rahman GMA, Zerbetto F, Prato M (2005) Carbon nanotubes in electron donor-acceptor nanocomposites. Acc Chem Res 38:871–878
Gust D, Moore TA, Moore AL (2000) Mimicking photosynthetic solar energy transduction. Acc Chem Res 34:40–48
Gust D, Moore TA, Moore AL (2009) Solar fuels via artificial photosynthesis. Acc Chem Res 42:1890–1898
Gutekunst K, Phunpruch S, Schwarz C, Schuchardt S, Schulz-Friedrich R, Appel J (2005) LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol Microbiol 58:810–823
Gutierrez-Sanchez C, Olea D, Marques M, Fernandez VM, Pereira IAC, Velez M, De Lacey AL (2011) Oriented immobilization of a membrane-bound hydrogenase onto an electrode for direct electron transfer. Langmuir 27:6449–6457
Gutthann F, Egert M, Marques A, Appel J (2007) Inhibition of respiration and nitrate assimilation enhances photohydrogen evolution under low oxygen concentrations in Synechocystis sp. PCC 6803. Biochim Biophys Acta 1767:161–169
Hall DO, Adams MWW, Morris P, Rao KK (1980) Photolysis of water for H2 production with the use of biological and artificial catalysts. Phil Trans R Soc A 295:473–476
Hambourger M, Liddell PA, Gust D, Moore AL, Moore TA (2007) Parameters affecting the chemical work output of a hybrid photoelectrochemical biofuel cell. Photochem Photobiol Sci 6:431–437
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 biofuel cell. J Am Chem Soc 130:2015–2022
Hambourger M, Kodis G, Vaughn MD, Moore GF, Gust D, Moore AL, Moore TA (2009) Solar energy conversion in a photoelectrochemical biofuel cell. Dalton Trans 45:9979–9989
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 (1993) 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
Happe RP, Roseboom W, Pierik AJ, Albracht SP, Bagley KA (1997) Biological activation of hydrogen. Nature 385:126
Hase T, Mizutani S, Mukohata Y (1991) Expression of maize Ferredoxin cDNA in Escherichia coli: comparison of photosynthetic and nonphotosynthetic ferredoxin isoproteins and their chimeric molecule. Plant Physiol 97:1395–1401
Haumann M, Liebisch P, Muller C, Barra M, Grabolle M, Dau H (2005) Photosynthetic O2 formation tracked by time-resolved X-ray experiments. Science 310:1019–1021
Heinekey DM (2009) Hydrogenase enzymes: recent structural studies and active site models. J Organomet Chem 694:2671–2680
Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926
Hiromoto T, Warkentin E, Moll J, Ermler U, Shima S (2009) The crystal structure of an [Fe]-hydrogenase-substrate complex reveals the framework for H2 activation. Angew Chem Int Ed Engl 48:6457–6460
Hoffmann D, Gutekunst K, Klissenbauer M, Schulz-Friedrich R, Appel J (2006) Mutagenesis of hydrogenase accessory genes of Synechocystis sp. PCC 6803. Additional homologues of hypA and hypB are not active in hydrogenase maturation. FEBS J 273:4516–4527
Howitt CA, Vermaas WFJ (1999) Subunits of the NAD(P)-reducing nickel-containing hydrogenase do not act as part of the type-1 NAD(P)H-dehydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. In: Peschek GA, Löffelhardt W, Schmetterer G (eds) The phototrophic prokaryotes. Springer, New York, pp 595–601
Ihara M, Nakamoto H, Kamachi T, Okura I, Maeda M (2006a) Photoinduced hydrogen production by direct electron transfer from photosystem I cross-linked with cytochrome c(3) to NiFe-hydrogenase. Photochem Photobiol 82:1677–1685
Ihara M, Nishihara H, Yoon KS, Lenz O, Friedrich B, Nakamoto H, Kojima K, Honma D, Kamachi T, Okura I (2006b) Light-driven hydrogen production by a hybrid complex of a NiFe-hydrogenase and the cyanobacterial photosystem I. Photochem Photobiol 82:676–682
Iwai M, Takizawa K, Tokutsu R, Okamuro A, Takahashi Y, Minagawa J (2010) Isolation of the elusive supercomplex that drives cyclic electron flow in photosynthesis. Nature 464:1210–1213
Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329
Jacquot JP, Stein M, Suzuki A, Liottet S, Sandoz G, Miginiac-Maslow M (1997) Residue Glu-91 of Chlamydomonas reinhardtii ferredoxin is essential for electron transfer to ferredoxin-thioredoxin reductase. FEBS Lett 400:293–296
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193
James B, Baum G, Perez J, Baum K (2008) Technoeconomic boundary analysis of biological pathways to hydrogen production. subcontract Report NREL/SR-560-46674:235–239
Jin RG, Richter S, Zhong R, Lamppa GK (2003) Expression and import of an active cellulase from a thermophilic bacterium into the chloroplast both in vitro and in vivo. Plant Mol Biol 51:493–507
Johnson X, Alric J (2012) Interaction between starch breakdown, acetate assimilation, and photosynthetic cyclic electron flow in Chlamydomonas reinhardtii. J Biol Chem 287:26445–26452
Joo H, Bae S, Kim C, Kim S, Yoon J (2009) Hydrogen evolution in enzymatic photoelectrochemical cell using modified seawater electrolytes produced by membrane desalination process. Sol Energy Mater Solar Cells 93:1555–1561
Kaluarachchi H, Zhang JW, Zamble DB (2011) Escherichia coli SlyD, more than a Ni(II) reservoir. Biochemistry 50:10761–10763
Kato M, Cardona T, Rutherford AW, Reisner E (2012) Photoelectrochemical water oxidation with photosystem II integrated in a mesoporous indium-tin oxide electrode. J Am Chem Soc 134:8332–8335
Keegstra K, Cline K (1999) Protein import and routing systems of chloroplasts. Plant Cell 11:557–570
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
Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817:158–166
Kirst H, Garcia-Cerdan JG, Zurbriggen A, Melis A (2012) Assembly of the light-harvesting chlorophyll antenna in the green alga Chlamydomonas reinhardtii requires expression of the TLA2-CpFTSY gene. Plant Physiol 158:930–945
Kiss E, Kos PB, Vass I (2009) Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. J Biotechnol 142:31–37
Knorzer P, Silakov A, Foster CE, Armstrong FA, Lubitz W, Happe T (2012) Importance of the protein framework for catalytic activity of [FeFe]-hydrogenases. J Biol Chem 287:1489–1499
Kondo T, Arakawa M, Hirai T, Wakayama T, Hara M, Miyake J (2002) Enhancement of hydrogen production by a photosynthetic bacterium mutant with reduced pigment. J Biosci Bioeng 93:145–150
Koprat J, Tottey S, Birkenbihl RP, Depège N, Hiujser P, Merchant S (2005) A regulator of nutritional copper signaling in Chlamydomonas is an SBP domain protein that recognizes the GTAC core of copper response element. Proc Natl Acad Sci U S A 102:18730–18735
Kosourov S, Seibert M (2008) 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, Seibert M, Ghirardi ML (2003) Effects of extracellular pH on the metabolic pathways in sulfur-deprived, H2-producing Chlamydomonas reinhardtii cultures. Plant Cell Physiol 44:146–155
Kosourov S, Ghirardi ML, Seibert M (2011) A truncated antenna mutant of Chlamydomonas reinhardtii can produce more hydrogen than the parental strain. Int J Hydrog Energy 36:2044–2048
Krassen H, Schwarze A, Friedrich B, Ataka K, Lenz O, Heberle J (2009) Photosynthetic hydrogen production by a hybrid complex of photosystem I and [NiFe] -hydrogenase. ACS Nano 3:4055–4061
Krassen H, Stripp ST, Bohm N, Berkessel A, Happe T, Ataka K, Heberle J (2011) Tailor-made modification of a gold surface for the chemical binding of a high-activity [FeFe] hydrogenase. Eur J Inorg Chem 2011:1138–1146
Krishnan S, Armstrong FA (2012) Order-of-magnitude enhancement of an enzymatic hydrogen-air fuel cell based on pyrenyl carbon nanostructures. Chem Sci 3:1015–1023
Kruse O, Hankamer B (2010) Microalgal hydrogen production. Curr Opin Biotechnol 21:238–243
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
Kuchenreuther JM, Grady-Smith CS, Bingham AS, George SJ, Cramer SP, Swartz JR (2010) High-yield expression of heterologous [FeFe] hydrogenases in Escherichia coli. PLoS One 5:e15491
Kuchenreuther JM, George SJ, Grady-Smith CS, Cramer SP, Swartz JR (2011) Cell-free H-cluster synthesis and [FeFe] hydrogenase activation: all five CO and CN(-) ligands derive from tyrosine. PLoS One 6:e20346
Kucho K, Okamoto K, Tsuchiya Y, Nomura S, Nango M, Kanehisa M, Ishiura M (2005) Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 187:2190–2199
Laffly E, Garzoni F, Fontecilla-Camps JC, Cavazza C (2010) Maturation and processing of the recombinant FeFe hydrogenase from Desulfovibrio vulgaris Hildenborough (DvH) in Escherichia coli. Int J Hydrog Energy 35:10761–10769
Lambertz C, Hemschemeier A, Happe T (2010) Anaerobic expression of the ferredoxin-encoding FDX5 gene of Chlamydomonas reinhardtii is regulated by the Crr1 transcription factor. Eukaryot Cell 9:1747–1754
Lambertz C, Leidel N, Havelius KGV, Noth J, Chernev P, Winkler M, Happe T, Haumann M (2011) O2 reactions at the six-iron active site (H-cluster) in [FeFe]-hydrogenase. J Biol Chem 286:40614–40623
Lambrev PH, Miloslavina Y, Jahns P, Holzwarth AR (2012) On the relationship between non-photochemical quenching and photoprotection of photosystem II. Biochim Biophys Acta 1817:760–769
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
Lauterbach L, Idris Z, Vincent KA, Lenz O (2011) Catalytic properties of the isolated diaphorase fragment of the NAD+-reducing [NiFe]-hydrogenase from Ralstonia eutropha. PLoS One 6:25939
Lautier T, Ezanno P, Baffert C, Fourmond V, Cournac L, Fontecilla-Camps JC, Soucaille P, Bertrand P, Meynial-Salles I, Leger C (2011) The quest for a functional substrate access tunnel in [FeFe] hydrogenase. Faraday Discuss 148:385–407
Lee JW, Greenbaum E (2003) A new oxygen sensitivity and its potential application in photosynthetic H2 production. Appl Biochem Biotechnol 105–108:303–313
Lee HS, Vermaas WF, Rittmann BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28:262–271
Leitao E, Pereira S, Bondoso J, Ferreira D, Pinto F, Moradas-Ferreira P, Tamagnini P (2006) Genes involved in the maturation of hydrogenase(s) in the nonheterocystous cyanobacterium Lyngbya majuscula CCAP 1446/4. Int J Hydrog Energy 31:1469–1477
Lemeille S, Turkina MV, Vener AV, Rochaix JD (2010) Stt7-dependent phosphorylation during state transitions in the green alga Chlamydomonas reinhardtii. Mol Cell Proteomics 9:1281–1295
Lemon BJ, Peters JW (2000) Photochemistry at the active site of the carbon monoxide inhibited form of the iron-only hydrogenase (CpI). J Am Chem Soc 122:3793–3794
Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260
Liebgott PP, Dementin S, Leger C, Rousset M (2011) Towards engineering O2-tolerance in Ni-Fe hydrogenases. Energy Environ Sci 4:33–41
Lojou E, Luo X, Brugna M, Candoni N, Dementin S, Giudici-Orticoni MT (2008) Biocatalysts for fuel cells: efficient hydrogenase orientation for H2 oxidation at electrodes modified with carbon nanotubes. J Biol Inorg Chem 13:1157–1167
Long M, Liu J, Chen Z, Bleijlevens B, Roseboom W, Albracht SP (2007) Characterization of a HoxEFUYH type of [NiFe] hydrogenase from Allochromatium vinosum and some EPR and IR properties of the hydrogenase module. J Biol Inorg Chem 12:62–78
Long H, Chang CH, King PW, Ghirardi ML, Kim K (2008) Brownian dynamics and molecular dynamics study of the association between hydrogenase and ferredoxin from Chlamydomonas reinhardtii. Biophys J 95:3753–3766
Long H, King PW, Ghirardi ML, Kim K (2009) Hydrogenase/ferredoxin charge-transfer complexes: effect of hydrogenase mutations on the complex association. J Phys Chem A 113:4060–4067
Lubitz W, Reijerse E, van Gastel M (2007) [NiFe] and [FeFe] hydrogenases studied by advanced magnetic resonance techniques. Chem Rev 107:4331–4365
Lubitz W, Reijerse EJ, Messinger J (2008) Solar water-splitting into H2 and O2: design principles of photosystem II and hydrogenases. Energy Environ Sci 1:15–31
Lubner CE, Knorzer P, Silva PJ, Vincent KA, Happe T, Bryant DA, Golbeck JH (2010) Wiring an [FeFe]-hydrogenase with photosystem I for light-induced hydrogen production. Biochemistry 49:10264–10266
Lubner CE, Applegate AM, Knorzer P, Ganago A, Bryant DA, Happe T, Golbeck JH (2011) Solar hydrogen-producing bionanodevice outperforms natural photosynthesis. Proc Natl Acad Sci U S A 108:20988–20991
Lutz S, Jacobi A, Schlensog V, Bohm R, Sawers G, Bock A (1991) Molecular characterization of an operon (hyp) necessary for the activity of the three hydrogenase isoenzymes in Escherichia coli. Mol Microbiol 5:123–135
Madden C, Vaughn MD, Diez-Perez I, Brown KA, King PW, Gust D, Moore AL, Moore TA (2012) Catalytic turnover of [FeFe] -hydrogenase based on single-molecule imaging. J Am Chem Soc 134:1577–1582
Magalon A, Bock A (2000) Dissection of the maturation reactions of the [NiFe] hydrogenase 3 from Escherichia coli taking place after nickel incorporation. FEBS Lett 473:254–258
Maier T, Jacobi A, Sauter M, Bock A (1993) The product of the hypB gene, which is required for nickel incorporation into hydrogenases, is a novel guanine nucleotide-binding protein. J Bacteriol 175:630–635
Markov AV, Gusakov AV, Dzedziulia EI, Ustinov BB, Antonov AA, Okunev ON, Bekkarevich AO, Sinitsyn AP (2006) Properties of hemicellulases of the enzyme complex from Trichoderma longibrachiatum. Prikl Biokhim Mikrobiol 42:654–664
Maroti J, Farkas A, Nagy IK, Maroti G, Kondorosi E, Rakhely G, Kovacs KL (2010) A second soluble Hox-type NiFe enzyme completes the hydrogenase set in Thiocapsa roseopersicina BBS. Appl Environ Microbiol 76:5113–5123
Massanz C, Schmidt S, Friedrich B (1998) Subforms and in vitro reconstitution of the NAD-reducing hydrogenase of Alcaligenes eutrophus. J Bacteriol 180:1023–1029
Matsubara H, Saeki K (1992) Structural and functional diversity of ferredoxins and related proteins. Adv Inorg Chem 38:223–280
Mazor Y, Toporik H, Nelson N (2012) Temperature-sensitive PSII and promiscuous PSI as a possible solution for sustainable photosynthetic hydrogen production. Biochim Biophys Acta 1817:1122–1126
McDonald TJ, Svedruzic D, Kim YH, Blackburn JL, Zhang SB, King PW, Heben MJ (2008) Wiring-up hydrogenase with single-walled carbon nanotubes. Nano Lett 7:3528–3534
McDonald AE, Ivanov AG, Bode R, Maxwell DP, Rodermel SR, Huner NP (2011) Flexibility in photosynthetic electron transport: the physiological role of plastoquinol terminal oxidase (PTOX). Biochim Biophys Acta 1807:954–967
McGlynn SE, Ruebush SS, Naumov A, Nagy LE, Dubini A, King PW, Broderick JB, Posewitz MC, Peters JW (2007) In vitro activation of [FeFe] hydrogenase: new insights into hydrogenase maturation. J Biol Inorg Chem 12:443–447
McGlynn SE, Shepard EM, Winslow MA, Naumov AV, Duschene KS, Posewitz MC, Broderick WE, Broderick JB, Peters JW (2008) HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis. FEBS Lett 582:2183–2187
McIntosh CL, Germer F, Schulz R, Appel J, Jones AK (2011) The [NiFe]-hydrogenase of the cyanobacterium Synechocystis sp. PCC 6803 works bidirectionally with a bias to H2 production. J Am Chem Soc 133:11308–11319
Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748
Melis A, Happe T (2004) Trails of green alga hydrogen research – from Hans Gaffron to new frontiers. Photosynth Res 80:401–409
Melis A, Neidhardt J, Benemann JR (1998) Dunaliella salina (Chlorophyta) with small chlorophyll antenna sizes exhibit higher photosynthetic productivities and photon use efficiencies than normally pigmented cells. J Appl Phycol 10:515–525
Melis A, Zhang L, 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 122:127–136
Merchant SS, Prochnik SE, Vallon O, Harris EH, Karpowicz SJ, Witman GB, Terry A, Salamov A, Fritz-Laylin LK, Marechal-Drouard L, Marshall WF, Qu LH, Nelson DR, Sanderfoot AA, Spalding MH, Kapitonov VV, Ren QH, Ferris P, Lindquist E, Shapiro H, Lucas SM, Grimwood J, Schmutz J, Cardol P, Cerutti H, Chanfreau G, Chen CL, Cognat V, Croft MT, Dent R, Dutcher S, Fernandez E, Fukuzawa H, Gonzalez-Ballester D, Gonzalez-Halphen D, Hallmann A, Hanikenne M, Hippler M, Inwood W, Jabbari K, Kalanon M, Kuras R, Lefebvre PA, Lemaire SD, Lobanov AV, Lohr M, Manuell A, Meir I, Mets L, Mittag M, Mittelmeier T, Moroney JV, Moseley J, Napoli C, Nedelcu AM, Niyogi K, Novoselov SV, Paulsen IT, Pazour G, Purton S, Ral JP, Riano-Pachon DM, Riekhof W, Rymarquis L, Schroda M, Stern D, Umen J, Willows R, Wilson N, Zimmer SL, Allmer J, Balk J, Bisova K, Chen CJ, Elias M, Gendler K, Hauser C, Lamb MR, Ledford H, Long JC, Minagawa J, Page MD, Pan JM, Pootakham W, Roje S, Rose A, Stahlberg E, Terauchi AM, Yang PF, Ball S, Bowler C, Dieckmann CL, Gladyshev VN, Green P, Jorgensen R, Mayfield S, Mueller-Roeber B, Rajamani S, Sayre RT, Brokstein P et al (2007) The Chlamydomonas genome reveals the evolution of key animal and plant functions. Science 318:245–251
Meuser JE, D’Adamo S, Jinkerson RE, Mus F, Yang WQ, Ghirardi ML, Seibert M, Grossman AR, Posewitz MC (2012) Genetic disruption of both Chlamydomonas reinhardtii [FeFe]-hydrogenases: insight into the role of HYDA2 in H2 production. Biochem Biophys Res Commun 417:704–709
Montet Y, Amara P, Volbeda A, Vernede X, Hatchikian EC, Field MJ, Frey M, Fontecilla-Camps JC (1997) Gas access to the active site of [NiFe] hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 4:523–526
Morra S, Valetti F, Sadeghi SJ, King PW, Meyer T, Gilardi G (2011) Direct electrochemistry of an FeFe -hydrogenase on a TiO2 electrode. Chem Commun (Camb) 47:10566–10568
Moulis JM, Davasse V (1995) Probing the role of electrostatic forces in the interaction of Clostridium pasteurianum ferredoxin with its redox partners. Biochemistry 34:16781–16788
Mulder DW, Ortillo DO, Gardenghi DJ, Naumov AV, Ruebush SS, Szilagyi RK, Huynh B, Broderick JB, Peters JW (2009) Activation of HydA(DeltaEFG) requires a preformed [4Fe-4S] cluster. Biochemistry 48:6240–6248
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(DeltaEFG). Nature 465:248–251
Mulder DW, Shepard EM, Meuser JE, Joshi N, King PW, Posewitz MC, Broderick JB, Peters JW (2011) Insights into [FeFe]-hydrogenase structure, mechanism, and maturation. Structure 19:1038–1052
Murthy UM, Wecker MS, Posewitz MC, Gilles-Gonzalez MA, Ghirardi ML (2012) Novel FixL homologues in Chlamydomonas reinhardtii bind heme and O2. FEBS Lett 586:4282–4288
Mus F, 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
Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9:503–510
Nakajima Y, Tsuzuki M, Ueda R (2001) Improved productivity by reduction of the content of light-harvesting pigment in Chlamydomonas perigranulata. J Appl Phycol 13:95–101
Navarro RM, Alvarez-Galvan MC, Villoria de la Mano JA, Al-Zahrani SM, Fierro JLG (2010) A framework for visible-light water splitting. Energy Environ Sci 3:1865–1882
Nicolet Y, Fontecilla-Camps JC (2012) Structure-function relationships in [FeFe]-hydrogenase active site maturation. J Biol Chem 287:13532–13540
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. Trends Biochem Sci 25:138–143
Nicolet Y, de Lacey AL, Vernede X, Fernandez VM, Hatchikian EC, Fontecilla-Camps JC (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 123:1596–1601
Nicolet Y, Rubach JK, Posewitz MC, Amara P, Mathevon C, Atta M, Fontecave M, Fontecilla-Camps JC (2008) X-ray structure of the [FeFe]-hydrogenase maturase HydE from Thermotoga maritima. J Biol Chem 283:18861–18872
Nicolet Y, Amara P, Mouesca JM, Fontecilla-Camps JC (2009) Unexpected electron transfer mechanism upon AdoMet cleavage in radical SAM proteins. Proc Natl Acad Sci U S A 106:14867–14871
Nicolet Y, Martin L, Tron C, Fontecilla-Camps JC (2010) A glycyl free radical as the precursor in the synthesis of carbon monoxide and cyanide by the [FeFe]-hydrogenase maturase HydG. FEBS Lett 584:4197–4202
Ogata H, Hirota S, Nakahara A, Komori H, Shibata N, Kato T, Kano K, Higuchi Y (2005) Activation process of [NiFe] hydrogenase elucidated by high-resolution X-ray analyses: conversion of the ready to the unready state. Structure 13:1635–1642
Ogata H, Lubitz W, Higuchi Y (2009) [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism. Dalton Trans 37:7577–7587
Oliveira P, Lindblad P (2005) LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol Lett 251:59–66
Oliveira P, Lindblad P (2008) An AbrB-like protein regulates the expression of the bidirectional hydrogenase in Synechocystis sp. strain PCC 6803. J Bacteriol 190:1011–1019
Oliveira P, Lindblad P (2009) Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. Dalton Trans 45:9990–9996
Oliveira P, Leitao E, Tamagnini P, Moradas-Ferreira P, Oxelfelt F (2004) Characterization and transcriptional analysis of hupSLW in Gloeothece sp. ATCC 27152: an uptake hydrogenase from a unicellular cyanobacterium. Microbiology 150:3647–3655
Olson JW, Maier RJ (1997) The sequences of hypF, hypC and hypD complete the hyp gene cluster required for hydrogenase activity in Bradyrhizobium japonicum. Gene 199:93–99
Olson JW, Maier RJ (2000) Dual roles of Bradyrhizobium japonicum nickelin protein in nickel storage and GTP-dependent Ni mobilization. J Bacteriol 182:1702–1705
Onda Y, Matsumura T, Kimata-Ariga Y, Sakakibara H, Sugiyama T, Hase T (2000) Differential interaction of maize root ferredoxin:NADP(+) oxidoreductase with photosynthetic and non-photosynthetic ferredoxin isoproteins. Plant Physiol 123:1037–1045
Ort DR, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85
Palagyi-Meszaros LS, Maroti J, Latinovics D, Balogh T, Klement E, Medzihradszky KF, Rakhely G, Kovacs KL (2009) Electron-transfer subunits of the [NiFe] hydrogenases in Thiocapsa roseopersicina BBS. FEBS J 276:164–174
Pandelia ME, Ogata H, Lubitz W (2010) Intermediates in the catalytic cycle of [NiFe] hydrogenase: functional spectroscopy of the active site. ChemPhysChem 11:1127–1140
Pandelia ME, Nitschke W, Infossi P, Giudici-Orticoni MT, Bill E, Lubitz W (2011) Characterization of a unique [FeS] cluster in the electron transfer chain of the oxygen tolerant [NiFe] hydrogenase from Aquifex aeolicus. Proc Natl Acad Sci U S A 108:6097–6102
Pandey AS, Harris TV, Giles LJ, Peters JW, Szilagyi RK (2008) Dithiomethylether as a ligand in the hydrogenase H-cluster. J Am Chem Soc 130:4533–4540
Papageorgiou GC, Tsimilli-Michael M, Stamatakis K (2007) The fast and slow kinetics of chlorophyll a fluorescence induction in plants, algae and cyanobacteria: a viewpoint. Photosynth Res 94:275–290
Pape M, Lambertz C, Happe T, Hemschemeier A (2012) Differential expression of the Chlamydomonas [FeFe]-hydrogenase-encoding HYDA1 gene Is regulated by the copper response regulator 1. Plant Physiol 159:1700–1712
Park HG, Holt JK (2010) Recent advances in nanoelectrode architecture for photochemical hydrogen production. Energy Environ Sci 3:1028–1036
Paschos A, Class RS, Bock A (2001) Carbamoyl phosphate requirement for synthesis of the active center of [NiFe]-hydrogenases. FEBS Lett 488:9–12
Pedroni P, Mura GM, Galli G, Pratesi C, Serbolisca L, Grandi G (1996) The hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus: from basic research to possible future applications. Int J Hydrog Energy 21:853–858
Peng XG (2010) Band gap and composition engineering on a nanocrystal (BCEN) in solution. Acc Chem Res 43:1387–1395
Peters JW (1999) Structure and mechanism of iron-only hydrogenases. Curr Opin Struct Biol 9:670–676
Peters JW, Broderick JB (2012) Emerging paradigms for complex iron-sulfur cofactor assembly and insertion. Annu Rev Biochem 81:429–450
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
Petroutsos D, Terauchi AM, Busch A, Hirschmann I, Merchant SS, Finazzi G, Hippler M (2009) PGRL1 Participates in iron-induced remodeling of the photosynthetic apparatus and in energy metabolism in Chlamydomonas reinhardtii. J Biol Chem 284:32770–32781
Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745
Pierik AJ, Hagen WR, Redeker JS, Wolbert RB, Boersma M, Verhagen MF, Grande HJ, Veeger C, Mutsaers PH, Sands RH et al (1992) Redox properties of the iron-sulfur clusters in activated Fe-hydrogenase from Desulfovibrio vulgaris (Hildenborough). Eur J Biochem 209:63–72
Pilet E, Nicolet Y, Mathevon C, Douki T, Fontecilla-Camps JC, Fontecave M (2009) The role of the maturase HydG in [FeFe]-hydrogenase active site synthesis and assembly. FEBS Lett 583:506–511
Pinto F, van Elburg KA, Pacheco CC, Lopo M, Noirel J, Montagud A, Urchueguia JF, Wright PC, Tamagnini P (2012) Construction of a chassis for hydrogen production: physiological and molecular characterization of a Synechocystis sp. PCC 6803 mutant lacking a functional bidirectional hydrogenase. Microbiology 158:448–464
Polle JEW, Kanakagiri SD, Melis A (2003) tla1, a DNA insertional transformant of the green alga Chlamydomonas reinhardtii with a truncated light-harvesting chlorophyll antenna size. Planta 217:49–59
Posewitz MC, King PW, Smolinski SL, Zhang L, Seibert M, Ghirardi ML (2004a) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720
Posewitz MC, Smolinski SL, Kanakagiri S, Melis A, Seibert M, Ghirardi ML (2004b) Hydrogen photoproduction is attenuated by disruption of an isoamylase gene in Chlamydomonas reinhardtii. Plant Cell 16:2151–2163
Posewitz MC, Dubini A, Meuser JE, Seibert M, Ghirardi ML (2008) Hydrogenases, hydrogen production, and anoxia. In: Stern D (ed) The Chlamydomonas sourcebook, vol 2, Organellar and metabolic processes. Academic, Oxford, UK, pp 217–255
Rakhely G, Kovacs AT, Maroti G, Fodor BD, Csanadi G, Latinovics D, Kovacs KL (2004) Cyanobacterial-type, heteropentameric, NAD+-reducing [NiFe] hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 70:722–728
Rakhely G, Laurinavichene TV, Tsygankov AA, Kovacs KL (2007) The role of Hox hydrogenase in the H2 metabolism of Thiocapsa roseopersicina. Biochim Biophys Acta 1767:671–676
Rao KK, Gogotov IN, Hall DO (1978) Hydrogen evolution by chloroplast-hydrogenase systems – improvements and additional observations. Biochimie 60:291–296
Reisner E (2011) Solar hydrogen evolution with hydrogenases: from natural to hybrid systems. Eur J Inorg Chem 2011:1005–1016
Reisner E, Fontecilla-Camps JC, Armstrong FA (2009a) Catalytic electrochemistry of a [NiFeSe]-hydrogenase on TiO2 and demonstration of its suitability for visible-light driven H2 production. Chem Commun (Camb) 5:550–552
Reisner E, Powell DJ, Cavazza C, Fontecilla-Camps JC, Armstrong FA (2009b) Visible light-driven H2 production by hydrogenases attached to dye-sensitized TiO2 nanoparticles. J Am Chem Soc 131:18457–18466
Reissmann S, Hochleitner E, Wang H, Paschos A, Lottspeich F, Glass RS, Bock A (2003) Taming of a poison: biosynthesis of the [NiFe]-hydrogenase cyanide ligands. Science 299:1067–1070
Roach PL (2011) Radicals from S-adenosylmethionine and their application to biosynthesis. Curr Opin Chem Biol 15:267–275
Roessler PG, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75:705–709
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
Rumeau D, Becuwe-Linka N, Beyly A, Louwagie M, Garin J, Peltier G (2005) New subunits NDH-M, -N, and -O, encoded by nuclear genes, are essential for plastid Ndh complex functioning in higher plants. Plant Cell 17:219–232
Rupprecht J (2009) From systems biology to fuel–Chlamydomonas reinhardtii as a model for a systems biology approach to improve biohydrogen production. J Biotechnol 142:10–20
Schmid B, Ribbe MW, Einsle O, Yoshida M, Thomas LM, Dean DR, Rees DC, Burgess BK (2002) Structure of a cofactor-deficient nitrogenase MoFe protein. Science 296:352–356
Schmitter JM, Jacquot JP, de Lamotte-Guery F, Beauvallet C, Dutka S, Gadal P, Decottignies P (1988) Purification, properties, and complete amino acid sequence of the ferredoxin from a green alga, Chlamydomonas reinhardtii. Eur J Biochem 172:405–412
Schmitz O, Boison G, Hilscher R, Hundeshagen B, Zimmer W, Lottspeich F, Bothe H (1995) Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. Eur J Biochem 233:266–276
Schmitz O, Boison G, Salzmann H, Bothe H, Schutz K, Wang SH, Happe T (2002) HoxE–a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta 1554:66–74
Schneider K, Cammack R, Schlegel HG (1984a) Content and localization of FMN, Fe-S clusters, and nickel in the NAD-linked hydrogenase of Nocardia opaca 1b. Eur J Biochem 142:75–84
Schneider K, Schlegel HG, Jochim K (1984b) Effect of nickel on activity and subunit composition of purified hydrogenase from Nocardia opaca 1b. Eur J Biochem 138:533–541
Schonfeld C, Wobbe L, Borgstadt R, Kienast A, Nixon PJ, Kruse O (2004) The nucleus-encoded protein MOC1 is essential for mitochondrial light acclimation in Chlamydomonas reinhardtii. J Biol Chem 279:50366–50374
Schutz K, Happe T, Troshina O, Lindblad P, Leitao E, Oliveira P, Tamagnini P (2004) Cyanobacterial H2 production – a comparative analysis. Planta 218:350–359
Selvaggi A, Tosi C, Barberini U, Franchi E, Rodriguez F, Pedroni P (1999) In vitro hydrogen photoproduction using Pyrococcus furiosus sulfhydrogenase and TiO2. J Photochem Photobiol 125:107–112
Serebriakova LT, Sheremetieva ME (2006) Characterization of catalytic properties of hydrogenase isolated from the unicellular cyanobacterium Gloeocapsa alpicola CALU 743. Biochemistry (Mosc) 71:1370–1376
Serebriakova LT, Zorin NA, Lindblad P (1994) Reversible hydrogenase in Anabaena variabilis ATCC29413 – presence and localization in non-N2-fixing cells. Arch Microbiol 161:140–144
Shepard EM, Duffus BR, George SJ, McGlynn SE, Challand MR, Swanson KD, Roach PL, Cramer SP, Peters JW, Broderick JB (2010a) [FeFe]-hydrogenase maturation: HydG-catalyzed synthesis of carbon monoxide. J Am Chem Soc 132:9247–9249
Shepard EM, McGlynn SE, Bueling AL, Grady-Smith CS, George SJ, Winslow MA, Cramer SP, Peters JW, Broderick JB (2010b) Synthesis of the 2Fe subcluster of the [FeFe]-hydrogenase H cluster on the HydF scaffold. Proc Natl Acad Sci U S A 107:10448–10453
Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217
Shomura Y, Higuchi Y (2012) Structural basis for the reaction mechanism of S-carbamoylation of HypE by HypF in the maturation of [NiFe]-hydrogenases. J Biol Chem 287:28409–28419
Shumilin IA, Nikandrov VV, Popov VO, Krasnovsky AA (1992) Photogeneration of NADH under coupled action of CdS semiconductor and hydrogenase from Alcaligenes eutrophus without exogenous mediators. FEBS Lett 306:125–128
Silakov A, Wenk B, Reijerse E, Lubitz W (2009) 14N HYSCORE investigation of the H-cluster of [FeFe] hydrogenase: evidence for a nitrogen in the dithiol bridge. Phys Chem Chem Phys 11:6592–6599
Silakov A, Olsen MT, Sproules S, Reijerse EJ, Rauchfuss TB, Lubitz W (2012) EPR/ENDOR, Mossbauer, and quantum-chemical investigations of diiron complexes mimicking the active oxidized state of [FeFe]-hydrogenase. Inorg Chem 51:8617–8628
Sjoholm J, Oliveira P, Lindblad P (2007) Transcription and regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. Appl Environ Microbiol 73:5435–5446
Stiebritz MT, Reiher M (2009) Theoretical study of dioxygen induced inhibition of [FeFe]-hydrogenase. Inorg Chem 48:7127–7140
Stiebritz MT, Reiher M (2012) Hydrogenases and oxygen. Chem Sci 3:1739–1751
Stirnberg M, Happe T (2004) Identification of a cis-acting element controlling anaerobic expression of the HYDA gene from Chlamydomonas reinhardtii. In: Jun M, Yasuo I, Rögner M (eds) Biohydrogen III. Elsevier Science, Amsterdam, pp 117–127
Stripp ST, Goldet G, Brandmayr C, Sanganas O, Vincent KA, Haumann M, Armstrong FA, Happe T (2009) How oxygen attacks [FeFe] hydrogenases from photosynthetic organisms. Proc Natl Acad Sci U S A 106:17331–17336
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
Tamagnini P, Leitao E, Oliveira P, Ferreira D, Pinto F, Harris DJ, Heidorn T, Lindblad P (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720
Teixeira VH, Baptista AM, Soares CM (2006) Pathways of H2 toward the active site of [NiFe]-hydrogenase. Biophys J 91:2035–2045
Terasaki N, Iwai M, Yamamoto N, Hiraga T, Yamada S, Inoue Y (2008) Photocurrent generation properties of Histag-photosystem II immobilized on nanostructured gold electrode. Thin Solid Films 516:2553–2557
Terauchi AM, Lu SF, Zaffagnini M, Tappa S, Hirasawa M, Tripathy JN, Knaff DB, Farmer PJ, Lemaire SD, Hase T, Merchant SS (2009) Pattern of expression and substrate specificity of chloroplast ferredoxins from Chlamydomonas reinhardtii. J Biol Chem 284:25867–25878
Thauer RK, Kaufer B, Zahringer M, Jungermann K (1974) The reaction of the iron-sulfur protein hydrogenase with carbon monoxide. Eur J Biochem 42:447–452
Thiemermann S, Dernedde J, Bernhard M, Schroeder W, Massanz C, Friedrich B (1996) Carboxyl-terminal processing of the cytoplasmic NAD-reducing hydrogenase of Alcaligenes eutrophus requires the hoxW gene product. J Bacteriol 178:2368–2374
Tibelius KH, Du L, Tito D, Stejskal F (1993) The Azotobacter chroococcum hydrogenase gene-cluster – sequences and genetic analysis of 4 accessory genes, HupA, HupB, HupY and HupC. Gene 127:53–61
Tolleter D, Ghysels B, Alric J, Petroutsos D, Tolstygina I, Krawietz D, Happe T, Auroy P, Adriano JM, Beyly A, Cuine S, Plet J, Reiter IM, Genty B, Cournac L, Hippler M, Peltier G (2011) Control of hydrogen photoproduction by the proton gradient generated by cyclic electron flow in Chlamydomonas reinhardtii. Plant Cell 23:2619–2630
Torzillo G, Scoma A, Faraloni C, Ena A, Johanningmeier U (2009) Increased hydrogen photoproduction by means of a sulfur-deprived Chlamydomonas reinhardtii D1 protein mutant. Int J Hydrog Energy 34:4529–4536
Tron C, Cherrier MV, Amara P, Martin L, Fauth F, Fraga E, Correard M, Fontecave M, Nicolet Y, Fontecilla Camps JC (2011) Further characterization of the [FeFe] hydrogenase maturase HydG. Eur J Inorg Chem 2011:1121–1127
Tsygankov AA (2007) Nitrogen-fixing cyanobacteria: a review. Appl Biochem Microbiol 43:250–259
Utschig LM, Silver SC, Mulfort KL, Tiede DM (2011) Nature-driven photochemistry for catalytic solar hydrogen production: a photosystem I transition metal catalyst hybrid. J Am Chem Soc 133:16334–16337
van der Spek TM, Arendsen AF, Happe RP, Yun S, Bagley KA, Stufkens DJ, Hagen WR, Albracht SP (1996) Similarities in the architecture of the active sites of Ni-hydrogenases and Fe-hydrogenases detected by means of infrared spectroscopy. Eur J Biochem 237:629–634
Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272
Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188
Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501
Vincent KA, Cracknell JA, Clark JR, Ludwig M, Lenz O, Friedrich B, Armstrong FA (2006) Electricity from low-level H2 in still air-an ultimate test for an oxygen tolerant hydrogenase. Chem Commun (Camb) 48:5033–5035
Vincent KA, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases. Chem Rev 107:4366–4413
Volbeda A, Martin L, Cavazza C, Matho M, Faber BW, Roseboom W, Albracht SPJ, Garcin E, Rousset M, Fontecilla-Camps JC (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10:239–249
Volbeda A, Amara P, Darnault C, Mouesca JM, Parkin A, Roessler MM, Armstrong FA, Fontecilla-Camps JC (2012) X-ray crystallographic and computational studies of the O2-tolerant [NiFe]-hydrogenase 1 from Escherichia coli. Proc Natl Acad Sci U S A 109:5305–5310
von Abendroth G, Stripp S, Silakov A, Croux C, Soucaille P, Girbal L, Happe T (2008) Optimized over-expression of [FeFe] hydrogenases with high specific activity in Clostridium acetobutylicum. Int J Hydrog Energy 33:6076–6081
Wang M, Chen L, Li X, Sun L (2011) Approaches to efficient molecular catalyst systems for photochemical H2 production using [FeFe]-hydrogenase active site mimics. Dalton Trans 40:12793–12800
Weyman PD, Vargas WA, Tong YK, Yu JP, Maness PC, Smith HO, Xu Q (2011) Heterologous expression of Alteromonas macleodii and Thiocapsa roseopersicina [NiFe} hydrogenases in Synechococcus elongatus. PLoS One 6:8
Winkler M, Hemschemeier A, Gotor C, Melis A, Happe T (2002) [Fe]-hydrogenases in green algae: photo-fermentation and hydrogen evolution under sulfur deprivation. Int J Hydrog Energy 27:1431–1439
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 284:36620–36627
Woolerton TW, Sheard S, Chaudhary YS, Armstrong FA (2012) Enzymes and bio-inspired electrocatalysts in solar fuel devices. Energy Environ Sci 5:7470–7490
Wunschiers R, Batur M, Lindblad P (2003) Presence and expression of hydrogenase specific C-terminal endopeptidases in cyanobacteria. BMC Microbiol 3:8
Yacoby I, Pochekailov S, Toporik H, Ghirardi ML, King PW, Zhang S (2011) Photosynthetic electron partitioning between [FeFe]-hydrogenase and ferredoxin:NADP+-oxidoreductase (FNR) enzymes in vitro. Proc Natl Acad Sci U S A 108:9396–9401
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:e35886
Yonekura-Sakakibara K, Onda Y, Ashikari T, Tanaka Y, Kusumi T, Hase T (2000) Analysis of reductant supply systems for ferredoxin-dependent sulfite reductase in photosynthetic and nonphotosynthetic organs of maize. Plant Physiol 122:887–894
Zadvornyy OA, Lucon JE, Gerlach R, Zorin NA, Douglas T, Elgren TE, Peters JW (2012) Photo-induced H2 production by [NiFe] -hydrogenase from T. roseopersicina covalently linked to a Ru(II) photosensitizer. J Inorg Biochem 106:151–155
Zhang JD, Chi Q, Kuznetsov AM, Hansen AG, Wackerbarth H, Christensen HEM, Andersen JET, Ulstrup J (2002) Electronic properties of functional biomolecules at metal/aqueous solution interfaces. J Phys Chem B 106:1131–1152
Zhang JD, Welinder AC, Chi QJ, Ulstrup J (2011) Electrochemically controlled self-assembled monolayers characterized with molecular and sub-molecular resolution. Phys Chem Chem Phys 13:5526–5545
Acknowledgements
The authors acknowledge financial support from DOE’s Office of Science’s Basic Energy Sciences (MLG, PWK, DWM) and Biological Environmental Research Programs (MLG, AD), EERE’s Fuel Cells Technology Office (MLG, PWK, PCM, JY), and ARPA-E (PCM, JY, CE). We are grateful for technical assistance from Dr. Damian Carrieri, Tameron Baldwin, and Lynn Westdal.
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2014 Springer Science+Business Media Dordrecht
About this chapter
Cite this chapter
Ghirardi, M.L. et al. (2014). Hydrogen Production by Water Biophotolysis. In: Zannoni, D., De Philippis, R. (eds) Microbial BioEnergy: Hydrogen Production. Advances in Photosynthesis and Respiration, vol 38. Springer, Dordrecht. https://doi.org/10.1007/978-94-017-8554-9_5
Download citation
DOI: https://doi.org/10.1007/978-94-017-8554-9_5
Published:
Publisher Name: Springer, Dordrecht
Print ISBN: 978-94-017-8553-2
Online ISBN: 978-94-017-8554-9
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)