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Hydrogen Production by Water Biophotolysis

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Microbial BioEnergy: Hydrogen Production

Part of the book series: Advances in Photosynthesis and Respiration ((AIPH,volume 38))

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.

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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

    CAS  PubMed  Google Scholar 

  • Adams MWW, Mortenson LE, Chen JS (1980) Hydrogenase. Biochim Biophys Acta 594:105–176

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Akhtar MK, Jones PR (2008) Engineering of a synthetic hydF-hydE-hydG-hydA operon for biohydrogen production. Anal Biochem 373:170–172

    CAS  PubMed  Google Scholar 

  • Akhtar MK, Jones PR (2009) Construction of a synthetic YdbK-dependent pyruvate:H2 pathway in Escherichia coli BL21(DE3). Metab Eng 11:139–147

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Allen JF (1992) Protein phosphorylation in regulation of photosynthesis. Biochim Biophys Acta 1098:275–335

    CAS  PubMed  Google Scholar 

  • Allen JF (2003) Cyclic, pseudocyclic and noncyclic photophosphorylation: new links in the chain. Trends Plant Sci 8:15–19

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Alric J (2010) Cyclic electron flow around photosystem I in unicellular green algae. Photosynth Res 106:47–56

    CAS  PubMed  Google Scholar 

  • Amirav L, Alivisatos AP (2010) Photocatalytic hydrogen production with tunable nanorod heterostructures. J Phys Chem Lett 1:1051–1054

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Armstrong FA, Heering HA, Hirst J (1997) Reactions of complex metalloproteins studied by protein-film voltammetry. Chem Soc Rev 26:169–179

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Axelsson R, Lindblad P (2002) Transcriptional regulation of Nostoc hydrogenases: effects of oxygen, hydrogen, and nickel. Appl Environ Microbiol 68:444–447

    CAS  PubMed Central  PubMed  Google Scholar 

  • Badia A, Lennox RB, Reven L (2000) A dynamic view of self-assembled monolayers. Acc Chem Res 33:475–481

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Blokesch M, Bock A (2002) Maturation of [NiFe]-hydrogenases in Escherichia coli: the HypC cycle. J Mol Biol 324:287–296

    CAS  PubMed  Google Scholar 

  • Bock A, King PW, Blokesch M, Posewitz MC (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bolton JR, Strickler SJ, Connolly JS (1985) Limiting and realizable efficiencies of solar photolysis of water. Nature 316:495–500

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Brand JJ, Wright JN, Lien S (1989) Hydrogen-production by eukaryotic algae. Biotechnol Bioeng 33:1482–1488

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Bruce BD (2000) Chloroplast transit peptides: structure, function and evolution. Trends Cell Biol 10:440–447

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Carrieri D, Wawrousek K, Eckert C, Yu J, Maness PC (2011) The role of the bidirectional hydrogenase in cyanobacteria. Bioresour Technol 102:8368–8377

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Chen XJ, Schnell DJ (1999) Protein import into chloroplasts. Trends Cell Biol 9:222–227

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Chen XB, Shen SH, Guo LJ, Mao SS (2010) Semiconductor-based photocatalytic hydrogen generation. Chem Rev 110:6503–6570

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Cracknell JA, Vincent KA, Armstrong FA (2008) Enzymes as working or inspirational electrocatalysts for fuel cells and electrolysis. Chem Rev 108:2439–2461

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ducat DC, Sachdeva G, Silver PA (2011) Rewiring hydrogenase-dependent redox circuits in cyanobacteria. Proc Natl Acad Sci U S A 108:3941–3946

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Eberhard S, Finazzi G, Wollman FA (2008) The dynamics of photosynthesis. Annu Rev Genet 42:463–515

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Elrad D, Niyogi KK, Grossman AR (2002) A major light-harvesting polypeptide of photosystem II functions in thermal dissipation. Plant Cell 14:1801–1816

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Eroglu E, Melis A (2011) Photobiological hydrogen production: recent advances and state of the art. Bioresour Technol 102:8403–8413

    CAS  PubMed  Google Scholar 

  • Esper B, Badura A, Rogner M (2006) Photosynthesis as a power supply for biohydrogen production. Trends Plant Sci 11:543–549

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Fontecilla-Camps JC, Volbeda A, Cavazza C, Nicolet Y (2007) Structure/function relationships of [NiFe]- and [FeFe]-hydrogenases. Chem Rev 107:4273–4303

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ghirardi ML, Togasaki R, Seibert M (1997) Oxygen sensitivity of algal H2-production. Appl Biochem Biotechnol 63–65:141–151

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ghirardi ML, Dubini A, Yu J, Maness PC (2009) Photobiological hydrogen-producing systems. Chem Soc Rev 38:52–61

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Guldi DM, Rahman GMA, Zerbetto F, Prato M (2005) Carbon nanotubes in electron donor-acceptor nanocomposites. Acc Chem Res 38:871–878

    CAS  PubMed  Google Scholar 

  • Gust D, Moore TA, Moore AL (2000) Mimicking photosynthetic solar energy transduction. Acc Chem Res 34:40–48

    Google Scholar 

  • Gust D, Moore TA, Moore AL (2009) Solar fuels via artificial photosynthesis. Acc Chem Res 42:1890–1898

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Happe RP, Roseboom W, Pierik AJ, Albracht SP, Bagley KA (1997) Biological activation of hydrogen. Nature 385:126

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Heinekey DM (2009) Hydrogenase enzymes: recent structural studies and active site models. J Organomet Chem 694:2671–2680

    CAS  Google Scholar 

  • Hemschemeier A, Happe T (2011) Alternative photosynthetic electron transport pathways during anaerobiosis in the green alga Chlamydomonas reinhardtii. Biochim Biophys Acta 1807:919–926

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Jacobs J, Pudollek S, Hemschemeier A, Happe T (2009) A novel, anaerobically induced ferredoxin in Chlamydomonas reinhardtii. FEBS Lett 583:325–329

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kaluarachchi H, Zhang JW, Zamble DB (2011) Escherichia coli SlyD, more than a Ni(II) reservoir. Biochemistry 50:10761–10763

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Keegstra K, Cline K (1999) Protein import and routing systems of chloroplasts. Plant Cell 11:557–570

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kirilovsky D, Kerfeld CA (2012) The orange carotenoid protein in photoprotection of photosystem II in cyanobacteria. Biochim Biophys Acta 1817:158–166

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Kiss E, Kos PB, Vass I (2009) Transcriptional regulation of the bidirectional hydrogenase in the cyanobacterium Synechocystis 6803. J Biotechnol 142:31–37

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • Kruse O, Hankamer B (2010) Microalgal hydrogen production. Curr Opin Biotechnol 21:238–243

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lee JW, Greenbaum E (2003) A new oxygen sensitivity and its potential application in photosynthetic H2 production. Appl Biochem Biotechnol 105–108:303–313

    PubMed  Google Scholar 

  • Lee HS, Vermaas WF, Rittmann BE (2010) Biological hydrogen production: prospects and challenges. Trends Biotechnol 28:262–271

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Li Z, Wakao S, Fischer BB, Niyogi KK (2009) Sensing and responding to excess light. Annu Rev Plant Biol 60:239–260

    CAS  PubMed  Google Scholar 

  • Liebgott PP, Dementin S, Leger C, Rousset M (2011) Towards engineering O2-tolerance in Ni-Fe hydrogenases. Energy Environ Sci 4:33–41

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Lubitz W, Reijerse E, van Gastel M (2007) [NiFe] and [FeFe] hydrogenases studied by advanced magnetic resonance techniques. Chem Rev 107:4331–4365

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Matsubara H, Saeki K (1992) Structural and functional diversity of ferredoxins and related proteins. Adv Inorg Chem 38:223–280

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Melis A, Happe T (2001) Hydrogen production. Green algae as a source of energy. Plant Physiol 127:740–748

    CAS  PubMed Central  PubMed  Google Scholar 

  • Melis A, Happe T (2004) Trails of green alga hydrogen research – from Hans Gaffron to new frontiers. Photosynth Res 80:401–409

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nakajima Y, Ueda R (1997) Improvement of photosynthesis in dense microalgal suspension by reduction of light harvesting pigments. J Appl Phycol 9:503–510

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Nicolet Y, Fontecilla-Camps JC (2012) Structure-function relationships in [FeFe]-hydrogenase active site maturation. J Biol Chem 287:13532–13540

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Nicolet Y, Lemon BJ, Fontecilla-Camps JC, Peters JW (2000) A novel FeS cluster in Fe-only hydrogenases. Trends Biochem Sci 25:138–143

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Ogata H, Lubitz W, Higuchi Y (2009) [NiFe] hydrogenases: structural and spectroscopic studies of the reaction mechanism. Dalton Trans 37:7577–7587

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Oliveira P, Lindblad P (2009) Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. Dalton Trans 45:9990–9996

    PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ort DR, Melis A (2011) Optimizing antenna size to maximize photosynthetic efficiency. Plant Physiol 155:79–85

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Park HG, Holt JK (2010) Recent advances in nanoelectrode architecture for photochemical hydrogen production. Energy Environ Sci 3:1028–1036

    CAS  Google Scholar 

  • Paschos A, Class RS, Bock A (2001) Carbamoyl phosphate requirement for synthesis of the active center of [NiFe]-hydrogenases. FEBS Lett 488:9–12

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • Peng XG (2010) Band gap and composition engineering on a nanocrystal (BCEN) in solution. Acc Chem Res 43:1387–1395

    CAS  PubMed  Google Scholar 

  • Peters JW (1999) Structure and mechanism of iron-only hydrogenases. Curr Opin Struct Biol 9:670–676

    CAS  PubMed  Google Scholar 

  • Peters JW, Broderick JB (2012) Emerging paradigms for complex iron-sulfur cofactor assembly and insertion. Annu Rev Biochem 81:429–450

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Philipps G, Happe T, Hemschemeier A (2012) Nitrogen deprivation results in photosynthetic hydrogen production in Chlamydomonas reinhardtii. Planta 235:729–745

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Rao KK, Gogotov IN, Hall DO (1978) Hydrogen evolution by chloroplast-hydrogenase systems – improvements and additional observations. Biochimie 60:291–296

    CAS  PubMed  Google Scholar 

  • Reisner E (2011) Solar hydrogen evolution with hydrogenases: from natural to hybrid systems. Eur J Inorg Chem 2011:1005–1016

    Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Roach PL (2011) Radicals from S-adenosylmethionine and their application to biosynthesis. Curr Opin Chem Biol 15:267–275

    CAS  PubMed  Google Scholar 

  • Roessler PG, Lien S (1984) Purification of hydrogenase from Chlamydomonas reinhardtii. Plant Physiol 75:705–709

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • Shikanai T (2007) Cyclic electron transport around photosystem I: genetic approaches. Annu Rev Plant Biol 58:199–217

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    PubMed Central  PubMed  Google Scholar 

  • Stiebritz MT, Reiher M (2009) Theoretical study of dioxygen induced inhibition of [FeFe]-hydrogenase. Inorg Chem 48:7127–7140

    CAS  PubMed  Google Scholar 

  • Stiebritz MT, Reiher M (2012) Hydrogenases and oxygen. Chem Sci 3:1739–1751

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Teixeira VH, Baptista AM, Soares CM (2006) Pathways of H2 toward the active site of [NiFe]-hydrogenase. Biophys J 91:2035–2045

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • Tsygankov AA (2007) Nitrogen-fixing cyanobacteria: a review. Appl Biochem Microbiol 43:250–259

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    PubMed  Google Scholar 

  • Vignais PM, Billoud B (2007) Occurrence, classification, and biological function of hydrogenases: an overview. Chem Rev 107:4206–4272

    CAS  PubMed  Google Scholar 

  • Vignais PM, Colbeau A (2004) Molecular biology of microbial hydrogenases. Curr Issues Mol Biol 6:159–188

    CAS  PubMed  Google Scholar 

  • Vignais PM, Billoud B, Meyer J (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol Rev 25:455–501

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Vincent KA, Parkin A, Armstrong FA (2007) Investigating and exploiting the electrocatalytic properties of hydrogenases. Chem Rev 107:4366–4413

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • Woolerton TW, Sheard S, Chaudhary YS, Armstrong FA (2012) Enzymes and bio-inspired electrocatalysts in solar fuel devices. Energy Environ Sci 5:7470–7490

    CAS  Google Scholar 

  • Wunschiers R, Batur M, Lindblad P (2003) Presence and expression of hydrogenase specific C-terminal endopeptidases in cyanobacteria. BMC Microbiol 3:8

    PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed Central  PubMed  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    CAS  PubMed  Google Scholar 

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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.

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  1. National Renewable Energy Laboratory, 15013 Denver West Parkway, Golden, CO, 80401, USA

    Maria L. Ghirardi, Paul W. King, David W. Mulder, Carrie Eckert, Alexandra Dubini, Pin-Ching Maness & Jianping Yu

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  1. Maria L. Ghirardi
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  2. Paul W. King
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  3. David W. Mulder
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Correspondence to Maria L. Ghirardi .

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  1. Dept. of Pharmacy and BioTechnology, University of Bologna, Bologna, Italy

    Davide Zannoni

  2. Dept. of AgriFood Production and Environmental Sciences, University of Florence, Florence, Italy

    Roberto De Philippis

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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

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