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Hydrogenases and Hydrogen Metabolism in Photosynthetic Prokaryotes

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Recent Advances in Phototrophic Prokaryotes

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 675))

Abstract

Hydrogen plays important, different roles in a variety of photosynthetic prokaryotes. The variety of different hydrogenases, their catalytic sites, maturation, and genetic organization are reviewed in the context of what is known about these enzymes from model non-photosynthetic organisms. Examples from specific cyanobacteria and various anoxygenic photosynthetic bacteria are discussed in detail along with what is known about their metabolic role. The latest findings on transcriptional regulators and the metabolic conditions that regulate the expression of hydrogenases in various photosynthetic prokaryotes are emphasized.

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References

  • Abdel-Basset R, Bader KP (1998) Physiological analyses of the hydrogen gas exchange in cyanobacteria. J Photochem Photobiol 43:146–151

    Article  CAS  Google Scholar 

  • Adams MW,Stiefel EI (1998) Biological hydrogen production: not so elementary. Science 282:1842–1843

    Article  CAS  PubMed  Google Scholar 

  • Agervald A, Stensjo K, Holmqvist M et al (2008) Transcription of the extended hyp-operon in Nostoc sp. strain PCC 7120. BMC Microbiol 8:69

    Article  PubMed  CAS  Google Scholar 

  • Alfonso M, Perewoska I, Kirilovsky D (2001) Redox control of ntcA gene expression in Synechocystis sp. PCC 6803. Nitrogen availability and electron transport regulate the levels of the NtcA protein. Plant Physiol 125:969–981

    Article  CAS  PubMed  Google Scholar 

  • Andrews SC, Berks BC, McClay J et al (1997) A 12-cistron Escherichia coli operon ( hyf) encoding a putative proton-translocating formate hydrogenlyase system. Microbiology 143 3633–3647

    Article  CAS  PubMed  Google Scholar 

  • Antal TK, Oliveira P Lindblad P (2006) The bidirectional hydrogenase in the cyanobacterium Synechocystis sp. strain PCC 6803. Int J Hydr Energ 31:1439–1444

    Article  CAS  Google Scholar 

  • Aoyama K, Uemura I, Miyake J et al (1997) Fermentative metabolism to produce hydrogen gas and organic compounds in a cyanobacterium, Spirulina platensis. J Ferment Bioeng 83:17–20

    Article  CAS  Google Scholar 

  • Aparicio PJ, Azuara MP, Ballesteros A et al (1985) Effects of light intensity and oxidized nitrogen sources on hydrogen production by Chlamydomonas reinhardtii. Plant Physiol 78:803–806

    Article  CAS  PubMed  Google Scholar 

  • Appel J, Phunpruch S, Steinmuller K et al (2000) The bidirectional hydrogenase of Synechocystis sp. PCC 6803 works as an electron valve during photosynthesis. Arch Microbiol 173:333–338

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Appel J, Schulz R (1998) Hydrogen metabolism in organisms with oxygenic photosynthesis: hydrogenases as important regulatory devices for a proper redox poising? J Photochem Photobiol B: Biology 47:1–11

    Article  CAS  Google Scholar 

  • Armstrong F A (2004) Hydrogenases: active site puzzles and progress. Curr Opin Chem Biol 8:133–140

    Article  CAS  PubMed  Google Scholar 

  • Armstrong FA, Albracht SP (2005) [NiFe]-hydrogenases: spectroscopic and electrochemical definition of reactions and intermediates. Philos Transact A Math Phys Eng Sci 363:937–954; discussion 1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Asen I, Djuranovic S, Lupas AN et al (2009) Crystal structure of SpoVT, the final modulator of gene expression during spore development in Bacillus subtilis. J Mol Biol 386:962–975

    Article  CAS  PubMed  Google Scholar 

  • Atanassova A, Zamble DB (2005) Escherichia coli HypA is a zinc metalloprotein with a weak affinity for nickel. J Bacteriol 187:4689–4697

    Article  CAS  PubMed  Google Scholar 

  • Atlung T, Knudsen K, Heerfordt L et al (1997) Effects of sigmaS and the transcriptional activator AppY on induction of the Escherichia coli hya and cbdAB- appA operons in response to carbon and phosphate starvation. J Bacteriol 179:2141–2146

    CAS  PubMed  Google Scholar 

  • Atlung T, Sund S, Olesen K et al (1996) The histone-like protein H-NS acts as a transcriptional repressor for expression of the anaerobic and growth phase activator AppY of Escherichia coli. J Bacteriol 178:3418–3425

    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

    Article  CAS  PubMed  Google Scholar 

  • Axelsson R, Oxelfelt F, Lindblad P (1999) Transcriptional regulation of Nostoc uptake hydrogenase. FEMS Microbiol Lett 170:77–81

    Article  CAS  PubMed  Google Scholar 

  • Bagramyan K, Trchounian A (2003) Structural and functional features of formate hydrogen lyase, an enzyme of mixed-acid fermentation from Escherichia coli. Biochemistry (Mosc) 68:1159–1170

    Article  CAS  Google Scholar 

  • Bagramyan K, Vassilian A, Mnatsakanyan N et al (2001) Participation of hyf-encoded hydrogenase 4 in molecular hydrogen release coupled with proton-potassium exchange in Escherichia coli. Membr Cell Biol 14:749–763

    CAS  PubMed  Google Scholar 

  • Bauer CE, Elsen S, Bird TH (1999) Mechanisms for redox control of gene expression. Annu Rev Microbiol 53:495–523

    Article  CAS  PubMed  Google Scholar 

  • Baumer S, Ide T, Jacobi C et al (2000) The F420H2 dehydrogenase from Methanosarcina mazei is a redox-driven proton pump closely related to NADH dehydrogenases. J Biol Chem 275:17968–17973

    Article  CAS  PubMed  Google Scholar 

  • Belkin S, Padan E, (1978) Hydrogen metabolism in the facultative anoxygenic cyanobacteria (blue-green algae) Oscillatoria limnetica and Aphanothece halophytica. Arch Microbiol 116:109–111

    Article  CAS  PubMed  Google Scholar 

  • Benemann JR Weare NM(1974) Hydrogen evolution by nitrogen-fixing Anabaena cylindrica cultures. Science 184:174–175

    Article  CAS  PubMed  Google Scholar 

  • Berks BC, Page MD, Richardson DJ et al (1995) Sequence analysis of subunits of the membrane-bound nitrate reductase from a denitrifying bacterium: the integral membrane subunit provides a prototype for the dihaem electron-carrying arm of a redox loop. Mol Microbiol 15:319–331

    Article  CAS  PubMed  Google Scholar 

  • Bernhard M, Buhrke T, Bleijlevens B et al (2001) The H2 sensor of Ralstonia eutropha. Biochemical characteristics, spectroscopic properties, and its interaction with a histidine protein kinase. J Biol Chem 276:15592–15597

    Article  CAS  PubMed  Google Scholar 

  • Black LK, Maier RJ, (1995) IHF- and RpoN-dependent regulation of hydrogenase expression in Bradyrhizobium japonicum. Mol Microbiol 16:405–413

    Article  CAS  PubMed  Google Scholar 

  • Bleijlevens B, Buhrke T, van der Linden E et al (2004) The auxiliary protein HypX provides oxygen tolerance to the soluble [NiFe]-hydrogenase of Ralstonia eutropha H16 by way of a cyanide ligand to nickel. J Biol Chem 279:46686–46691

    Article  CAS  PubMed  Google Scholar 

  • Blokesch M, Albracht SP, Matzanke BF et al (2004) The complex between hydrogenase-maturation proteins HypC and HypD is an intermediate in the supply of cyanide to the active site iron of [NiFe]-hydrogenases. J Mol Biol 344:155–167

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Blokesch M, Magalon A, Bock A (2001) Interplay between the specific chaperone-like proteins HybG and HypC in maturation of hydrogenases 1, 2, and 3 from Escherichia coli. J Bacteriol 183:2817–2822

    Article  CAS  PubMed  Google Scholar 

  • Bobay BG, Andreeva A, Mueller GA et al (2005) Revised structure of the AbrB N-terminal domain unifies a diverse superfamily of putative DNA-binding proteins. FEBS Lett 579:5669–5674

    Article  CAS  PubMed  Google Scholar 

  • Bobay BG, Benson L, Naylor S et al (2004) Evaluation of the DNA binding tendencies of the transition state regulator AbrB. Biochemistry 43:16106–16118

    Article  CAS  PubMed  Google Scholar 

  • Böck A, King PW, Blokesch M et al (2006) Maturation of hydrogenases. Adv Microb Physiol 51:1–71

    Article  PubMed  CAS  Google Scholar 

  • Böck A, Sawers G (1996) Fermentation. ASM Press, Washington, DC

    Google Scholar 

  • Bogorov LV (1974) The properties of Thiocapsa roseopersicina, strain BBS, isolated from an estuary of the white sea. Mikrobioloiia 43:326–332

    CAS  Google Scholar 

  • Bohm R, Sauter M, Bock A (1990) Nucleotide sequence and expression of an operon in Escherichia coli coding for formate hydrogenlyase components. Mol Microbiol 4:231–243

    Article  CAS  PubMed  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

    Article  CAS  PubMed  Google Scholar 

  • Bonam D, Lehman L, Roberts GP et al (1989) Regulation of carbon monoxide dehydrogenase and hydrogenase in Rhodospirillum rubrum: effects of CO and oxygen on synthesis and activity. J Bacteriol 171:3102–3107

    CAS  PubMed  Google Scholar 

  • Bonam D, Ludden PW (1987) Purification and characterization of carbon monoxide dehydrogenase, a nickel, zinc, iron-sulfur protein, from Rhodospirillum rubrum. J Biol Chem 262:2980–2987

    CAS  PubMed  Google Scholar 

  • Boyer ME, Stapleton JA, Kuchenreuther JM et al (2008) Cell-free synthesis and maturation of [FeFe] hydrogenases. Biotechnol Bioeng 99:59–67

    Article  CAS  PubMed  Google Scholar 

  • Brazzolotto X, Rubach JK, Gaillard J et al (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

    Article  CAS  PubMed  Google Scholar 

  • Brito B, Martinez M, Fernandez D et al (1997) Hydrogenase genes from Rhizobium leguminosarum bv. viciae are controlled by the nitrogen fixation regulatory protein nifA. Proc Natl Acad Sci USA 94:6019–6024

    Article  CAS  PubMed  Google Scholar 

  • Brito B, Toffanin A, Prieto RI et al (2008) Host-dependent expression of Rhizobium leguminosarum bv. viciae hydrogenase is controlled at transcriptional and post-transcriptional levels in legume nodules. Mol Plant Microbe Interact 21:597–604

    Article  CAS  PubMed  Google Scholar 

  • Brondsted L, Atlung T (1996) Effect of growth conditions on expression of the acid phosphatase ( cyx-appA) operon and the appY gene, which encodes a transcriptional activator of Escherichia coli. J Bacteriol 178:1556–1564

    CAS  PubMed  Google Scholar 

  • Bryant MP, Wolin EA, Wolin MJ et al (1967) Methanobacillus omelianskii, a symbiotic association of two species of bacteria. Arch Mikrobiol 59:20–31

    Article  CAS  PubMed  Google Scholar 

  • Buhrke T, Lenz O, Krauss N et al (2005) Oxygen tolerance of the H2-sensing [NiFe] hydrogenase from Ralstonia eutropha H16 is based on limited access of oxygen to the active site. J Biol Chem 280:23791–23796

    Article  CAS  PubMed  Google Scholar 

  • Buhrke T, Lenz O, Porthun A et al (2004) The H2-sensing complex of Ralstonia eutropha: interaction between a regulatory [NiFe] hydrogenase and a histidine protein kinase. Mol Microbiol 51:1677–1689

    Article  CAS  PubMed  Google Scholar 

  • Chou CJ, Jenney FE, Jr, Adams MW et al (2008) Hydrogenesis in hyperthermophilic microorganisms: implications for biofuels. Metab Eng 10:394–404

    Article  CAS  PubMed  Google Scholar 

  • Colbeau A, Kelley BC, Vignais PM (1980) Hydrogenase activity in Rhodopseudomonas capsulata: relationship with nitrogenase activity. J Bacteriol 144:141–148

    CAS  PubMed  Google Scholar 

  • Colbeau A, Kovacs KL, Chabert J et al (1994) Cloning and sequence of the structural ( hupSLC) and accessory ( hupDHI) genes for hydrogenase biosynthesis in Thiocapsa roseopersicina. Gene 140:25–31

    Article  CAS  PubMed  Google Scholar 

  • Coles M, Djuranovic S, Soding J et al (2005) AbrB-like transcription factors assume a swapped hairpin fold that is evolutionarily related to double-psi beta barrels. Structure 13:919–928

    Article  CAS  PubMed  Google Scholar 

  • Conrad R (1996) Soil microorganisms as controllers of atmospheric trace gases (H2, CO, CH4, OCS, N2O, and NO). Microbiol Rev 60:609–640

    CAS  PubMed  Google Scholar 

  • Cooley JW, Vermaas WF (2001) Succinate dehydrogenase and other respiratory pathways in thylakoid membranes of Synechocystis sp. strain PCC 6803: capacity comparisons and physiological function. J Bacteriol 183:4251–4258

    Article  CAS  PubMed  Google Scholar 

  • Cournac L, Guedeney G, Peltier G et al (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

    Article  CAS  PubMed  Google Scholar 

  • Dahl C, Rakhely G, Pott-Sperling AS et al (1999) Genes involved in hydrogen and sulfur metabolism in phototrophic sulfur bacteria. FEMS Microbiol Lett 180:317–324

    Article  CAS  PubMed  Google Scholar 

  • Dementin S, Leroux F, Cournac L et al (2009) Introduction of methionines in the gas channel makes [NiFe] hydrogenase aero-tolerant. J Am Chem Soc 131:10156–10164

    Article  CAS  PubMed  Google Scholar 

  • Devine E, Holmqvist M, Stensjo K et al (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

    Article  PubMed  CAS  Google Scholar 

  • Dias AV, Mulvihill CM, Leach MR et al (2008) Structural and biological analysis of the metal sites of Escherichia coli hydrogenase accessory protein HypB. Biochemistry 47:11981–11991

    Article  CAS  PubMed  Google Scholar 

  • Dischert W, Vignais PM, Colbeau A (1999) The synthesis of Rhodobacter capsulatus HupSL hydrogenase is regulated by the two-component HupT/HupR system. Mol Microbiol 34:995–1006

    Article  CAS  PubMed  Google Scholar 

  • Domain F, Houot L, Chauvat F et al (2004) Function and regulation of the cyanobacterial genes lexA, recA and ruvB: LexA is critical to the survival of cells facing inorganic carbon starvation. Mol Microbiol 53:65–80

    Article  CAS  PubMed  Google Scholar 

  • Drapal N, Bock A (1998) Interaction of the hydrogenase accessory protein HypC with HycE, the large subunit of Escherichia coli hydrogenase 3 during enzyme maturation. Biochemistry 37:2941–2948

    Article  CAS  PubMed  Google Scholar 

  • Drennan CL, Heo J, Sintchak MD et al (2001) Life on carbon monoxide: X-ray structure of Rhodospirillum rubrum Ni-Fe-S carbon monoxide dehydrogenase. Proc Natl Acad Sci USA 98:11973–11978

    Article  CAS  PubMed  Google Scholar 

  • Drutschmann M, Klemme JH (1985) Sulfide repressed, membrane bound hydrogenase in the thermophilic facultative phototroph, Chlorojiexus aurantiacus. FEMS Microbiology Letters 28:231–235

    Article  CAS  Google Scholar 

  • Duche O, Elsen S, Cournac L et al (2005) Enlarging the gas access channel to the active site renders the regulatory hydrogenase HupUV of Rhodobacter capsulatus O2 sensitive without affecting its transductory activity. Febs J 272:3899–3908

    Article  PubMed  Google Scholar 

  • Durmowicz M, Maier R (1997) Roles of HoxX and HoxA in biosynthesis of hydrogenase in Bradyrhizobium japonicum. J Bacteriol 179:3676–3682

    CAS  PubMed  Google Scholar 

  • Durmowicz MC, Maier RJ (1998) The FixK2 protein is involved in regulation of symbiotic hydrogenase expression in Bradyrhizobium japonicum. J Bacteriol 180:3253–3256

    CAS  PubMed  Google Scholar 

  • Eisen JA, Karen EN, Paulsen IT et al (2002) The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci USA. 99:9509–9514

    Article  CAS  PubMed  Google Scholar 

  • Eisbrenner G, Distler E, Floener L et al (1978) The occurrence of the hydrogenase in cyanobacteria. Archives of Microbiology 118:177–184

    Article  CAS  Google Scholar 

  • Elsen S, Dischert W, Colbeau A et al (2000) Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system. J Bacteriol 182:2831–2837

    Article  CAS  PubMed  Google Scholar 

  • Ensign SA, Ludden PW (1991) Characterization of the CO oxidation/H2 evolution system of Rhodospirillum rubrum. Role of a 22-kDa iron-sulfur protein in mediating electron transfer between carbon monoxide dehydrogenase and hydrogenase. J Biol Chem 266:18395–18403

    CAS  PubMed  Google Scholar 

  • Espinosa J, Forchhammer K, Burillo S et al (2006) Interaction network in cyanobacterial nitrogen regulation: PipX, a protein that interacts in a 2-oxoglutarate dependent manner with PII and NtcA. Mol Microbiol 61:457–469

    Article  CAS  PubMed  Google Scholar 

  • Fay P (1992) Oxygen relations of nitrogen fixation in cyanobacteria. Microbiol Rev 56:340–373

    CAS  PubMed  Google Scholar 

  • Fernández VM, Aguirre R, Hatchikian EC (1984) Reductive activation and redox properties of hydrogenase from Desulfovibrio gigas. Biochim Biophys Acta 790:1–797

    Article  Google Scholar 

  • Fernandez VM, Hatchikian EC, Cammack R (1985) Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase. Biochim Biophys Acta 832:69–79

    Article  CAS  Google Scholar 

  • Ferreira D, Leitao E, Sjoholm J et al (2007) Transcription and regulation of the hydrogenase(s) accessory genes, hypFCDEAB, in the cyanobacterium Lyngbya majuscula CCAP 1446/4. Arch Microbiol 188:609–617

    Article  CAS  PubMed  Google Scholar 

  • Ferreira D, Pinto F, Moradas-Ferreira P et al (2009) Transcription profiles of hydrogenases related genes in the cyanobacterium Lyngbya majuscula CCAP 1446/4. BMC Microbiol 9:67

    Article  PubMed  CAS  Google Scholar 

  • Finlay BJ, Fenchel T (1992) An anaerobic ciliate as a natural chemostat for the growth of endosymbiotic methanogens. Eur J Protistol. 28:127–137

    Article  CAS  PubMed  Google Scholar 

  • Fontecave M, Ollagnier-de-Choudens S, Mulliez E (2003) Biological radical sulfur insertion reactions. Chem Rev 103:2149–2166

    Article  CAS  PubMed  Google Scholar 

  • Fontecilla-Camps JC, Frey M, Garcin E et al (1997) Hydrogenase: a hydrogen-metabolizing enzyme. What do the crystal structures tell us about its mode of action? Biochimie 79:661–666

    Article  CAS  PubMed  Google Scholar 

  • Forchhammer K. (2007) Glutamine signalling in bacteria. Front Biosci 12:358–370

    Article  CAS  PubMed  Google Scholar 

  • Forzi L, Sawers RG (2007) Maturation of [NiFe]-hydrogenases in Escherichia coli. Biometals 20:565–578

    Article  CAS  PubMed  Google Scholar 

  • Fox JD, He Y, Shelver D et al (1996) Characterization of the region encoding the CO-induced hydrogenase of Rhodospirillum rubrum. J Bacteriol 178:6200–6208

    CAS  PubMed  Google Scholar 

  • Frenkel A, Gaffron H, Battley EH(1950) Photosynthesis and photoreduction by the blue green alga, Synechococcus elongatus, Nag. Biol Bull 99:157–162

    Article  CAS  PubMed  Google Scholar 

  • Friedrich B, Buhrke T, Burgdorf T et al (2005) A hydrogen-sensing multiprotein complex controls aerobic hydrogen metabolism in Ralstonia eutropha. Biochem Soc Trans 33:97–101

    Article  CAS  PubMed  Google Scholar 

  • Fritsche E, Paschos A, Beisel HG et al (1999) Crystal structure of the hydrogenase maturating endopeptidase HybD from Escherichia coli. J Mol Biol 288:989–998

    Article  CAS  PubMed  Google Scholar 

  • Garcin E, Vernede X, Hatchikian EC et al (1999) The crystal structure of a reduced [NiFeSe] hydrogenase provides an image of the activated catalytic center. Structure 7:557–566

    Article  CAS  PubMed  Google Scholar 

  • Gasper R, Scrima A, Wittinghofer A (2006) Structural insights into HypB, a GTP-binding protein that regulates metal binding. J Biol Chem 281:27492–27502

    Article  CAS  PubMed  Google Scholar 

  • George SJ, Kurkin S, Thorneley RN et al (2004) Reactions of H2, CO, and O2 with active [NiFe]-hydrogenase from Allochromatium vinosum. A stopped-flow infrared study. Biochemistry 43:6808–6819

    Article  CAS  PubMed  Google Scholar 

  • Germer F, Zebger I, Saggu M et al (2009) Overexpression, isolation and spectroscopic characterization of the bidirectional [NiFe]-hydrogenase from Synechocystis sp. PCC 6803. J Biol Chem 284:36462–36472

    Article  CAS  PubMed  Google Scholar 

  • Giese KC, Michalowski CB, Little JW (2008) RecA-dependent cleavage of LexA dimers. J Mol Biol 377:148–161

    Article  CAS  PubMed  Google Scholar 

  • Gogotov IN, Zorin NA, Serebriakova LT et al (1978) The properties of hydrogenase from Thiocapsa roseopersicina. Biochim Biophys Acta 523:335–343

    Article  CAS  PubMed  Google Scholar 

  • Green J, Bennett B, Jordan P et al (1996) Reconstitution of the [4Fe-4S] cluster in FNR and demonstration of the aerobic-anaerobic transcription switch in vitro. Biochem J 316 (Pt 3): 887–892

    CAS  PubMed  Google Scholar 

  • Gutekunst K, Hoffmann D, Lommer M et al (2006) Metal dependence and intracellular regulation of the bidirectional NiFe–hydrogenase in Synechocystis sp. PCC 6803. IntJHydrEnerg 31:1452–1459

    CAS  Google Scholar 

  • Gutekunst K, Phunpruch S, Schwarz C et al (2005) LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol Microbiol 58:810–823

    Article  CAS  PubMed  Google Scholar 

  • Gutierrez D, Hernando Y, Palacios JM et al (1997) FnrN controls symbiotic nitrogen fixation and hydrogenase activities in Rhizobium leguminosarum biovar viciae UPM791. J Bacteriol 179:5264–5270

    CAS  PubMed  Google Scholar 

  • Gutthann F, Egert M, Marques A et al (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

    Article  CAS  PubMed  Google Scholar 

  • Hackstein JH, Akhmanova A, Boxma B et al (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol 7:441–447

    Article  CAS  PubMed  Google Scholar 

  • Hallenbeck PC (2005) Fundamentals of the fermentative production of hydrogen. Water Sci Technol 52:21–29

    CAS  PubMed  Google Scholar 

  • Happe RP, Roseboom W, Pierik AJ et al (1997) Biological activation of hydrogen. Nature 385:126

    Article  CAS  PubMed  Google Scholar 

  • Happe T, Hemschemeier A, Winkler M et al (2002) Hydrogenases in green algae: do they save the algae’s life and solve our energy problems? Trends Plant Sci 7:246–250

    Article  CAS  PubMed  Google Scholar 

  • Happe T, Schutz K, Bohme H (2000) Transcriptional and mutational analysis of the uptake hydrogenase of the filamentous cyanobacterium Anabaena variabilis ATCC 29413. J Bacteriol 182:1624–1631

    Article  CAS  PubMed  Google Scholar 

  • Hayes ET, Wilks JC, Sanfilippo P et al (2006) Oxygen limitation modulates pH regulation of catabolism and hydrogenases, multidrug transporters, and envelope composition in Escherichia coli K-12. BMC Microbiol 6:89

    Article  PubMed  CAS  Google Scholar 

  • Hedderich R, Forzi L (2005) Energy-converting [NiFe] hydrogenases: more than just H2 activation. J Mol Microbiol Biotechnol 10:92–104

    Article  CAS  PubMed  Google Scholar 

  • Heo J, Halbleib CM Ludden PW (2001) Redox-dependent activation of CO dehydrogenase from Rhodospirillum rubrum. Proc Natl Acad Sci USA 98:7690–7693

    Article  CAS  PubMed  Google Scholar 

  • Heo J, Wolfe MT, Staples CR et al (2002) Converting the NiFeS carbon monoxide dehydrogenase to a hydrogenase and a hydroxylamine reductase. J Bacteriol 184:5894–5897

    Article  CAS  PubMed  Google Scholar 

  • Herrero A, Muro-Pastor AM,Flores E (2001) Nitrogen control in cyanobacteria. J Bacteriol 183:411–425

    Article  CAS  PubMed  Google Scholar 

  • Hidalgo E, Bollinger JM, Jr, Bradley TM et al (1995) Binuclear [2Fe-2S] clusters in the Escherichia coli SoxR protein and role of the metal centers in transcription. J Biol Chem 270:20908–20914

    Article  CAS  PubMed  Google Scholar 

  • Higuchi Y, Yagi T, Yasuoka N (1997) Unusual ligand structure in Ni-Fe active center and an additional Mg site in hydrogenase revealed by high resolution X-ray structure analysis. Structure 5:1671–1680

    Article  CAS  PubMed  Google Scholar 

  • Hoehler TM, Albert DB, Alperin MJ et al (2002) Comparative ecology of H2 cycling in sedimentary and phototrophic ecosystems. Antonie Van Leeuwenhoek 81:575–585

    Article  CAS  PubMed  Google Scholar 

  • Hoehler TM, Bebout B.M, Des Marais DJ (2001) The role of microbial mats in the production of reduced gases on the early Earth. Nature 412:324–327

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann D, Gutekunst K, Klissenbauer M et al (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

    Article  CAS  PubMed  Google Scholar 

  • Holmqvist M, Stensjo K, Oliveira P et al (2009) Characterization of the hupSL promoter activity in Nostoc punctiforme ATCC 29133. BMC Microbiol 9:54

    Article  PubMed  CAS  Google Scholar 

  • Houchins JP (1984) The physiology and biochemistry of hydrogen metabolism in cyanobacteria. Biochim Biophys Acta 768:227–255

    Article  CAS  Google Scholar 

  • Houchins JP, Burris RH (1981) Physiological Reactions of the Reversible Hydrogenase from Anabaena 7120. Plant Physiol 68:717–721

    Article  CAS  PubMed  Google Scholar 

  • Huang CJ, 1. Barrett EL (1991) Sequence analysis and expression of the Salmonella typhimurium asr operon encoding production of hydrogen sulfide from sulfite. J Bacteriol 173:1544–1553

    CAS  PubMed  Google Scholar 

  • Hube M, Blokesch M, Bock A (2002) Network of hydrogenase maturation in Escherichia coli: role of accessory proteins HypA and HybF. J Bacteriol 184:3879–3885

    Article  CAS  PubMed  Google Scholar 

  • Ishii A, Hihara Y (2008) An AbrB-like transcriptional regulator, Sll0822, is essential for the activation of nitrogen-regulated genes in Synechocystis sp. PCC 6803. Plant Physiol 148:660–670

    Article  CAS  PubMed  Google Scholar 

  • Jiang F, Mannervik B, Bergman B. (1997) Evidence for redox regulation of the transcription factor NtcA, acting both as an activator and a repressor, in the cyanobacterium Anabaena PCC 7120. Biochem J 327 (Pt 2): 513–517

    CAS  PubMed  Google Scholar 

  • Johnson DC, Dean DR, Smith AD et al (2005) Structure, function, and formation of biological iron-sulfur clusters. Annu Rev Biochem 74:247–281

    Article  CAS  PubMed  Google Scholar 

  • Jormakka M, Tornroth S, Byrne B et al (2002) Molecular basis of proton motive force generation: structure of formate dehydrogenase-N. Science 295:1863–1868

    Article  PubMed  Google Scholar 

  • Kerby RL, Hong SS, Ensign SA et al (1992) Genetic and physiological characterization of the Rhodospirillum rubrum carbon monoxide dehydrogenase system. J Bacteriol 174:5284–5294

    CAS  PubMed  Google Scholar 

  • Kerby RL, Ludden PW, Roberts GP (1995) Carbon monoxide-dependent growth of Rhodospirillum rubrum. J Bacteriol 177:2241–2244

    CAS  PubMed  Google Scholar 

  • Kiley PJ, Beinert H (1998) Oxygen sensing by the global regulator, FNR: the role of the iron-sulfur cluster. FEMS Microbiol Rev 22:341–352

    Article  CAS  PubMed  Google Scholar 

  • King PW, Posewitz MC, Ghirardi ML et al (2006) Functional studies of [FeFe] hydrogenase maturation in an Escherichia coli biosynthetic system. J Bacteriol 188:2163–2172

    Article  CAS  PubMed  Google Scholar 

  • King PW, Przybyla AE (1999) Response of hya expression to external pH in Escherichia coli. J Bacteriol 181:5250–5256

    CAS  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

    Article  CAS  PubMed  Google Scholar 

  • Kovacs AT, Rakhely G, Balogh J et al (2005) Hydrogen independent expression of hupSL genes in Thiocapsa roseopersicina BBS. Febs J 272:4807–4816

    Article  CAS  PubMed  Google Scholar 

  • Kovacs KL, Bagyinka C (1990) Structural properties, functional states and physiological roles of hydrogenase in photosynthetic bacteria. FEMS Microbiol. Rev. 87:407–412

    Article  CAS  Google Scholar 

  • Kovacs KL, Bagyinka C Serebriakova LT (1983) Distribution and orientation of hydrogenase in various photosynthetic bacteria. Current Microbiology 9:215–218

    Article  CAS  Google Scholar 

  • Kovács KL, Maróti G, Rákhely G (2006) A novel approach for biohydrogen production. Int J Hydrogen Energy 31:1460–1468

    Article  CAS  Google Scholar 

  • Kucho K, Okamoto K, Tsuchiya Y et al (2005) Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 187:2190–2199

    Article  CAS  PubMed  Google Scholar 

  • Kumarevel T, Tanaka T, Bessho Y et al (2009) Crystal structure of hydrogenase maturating endopeptidase HycI from Escherichia coli. Biochem Biophys Res Commun 389:310–314

    Article  CAS  PubMed  Google Scholar 

  • Kunkel A, Vorholt JA, Thauer RK et al (1998) An Escherichia coli hydrogenase-3-type hydrogenase in methanogenic archaea. Eur J Biochem 252:467–476

    Article  CAS  PubMed  Google Scholar 

  • Kurkin S, George SJ, Thorneley RN et al (2004) Hydrogen-induced activation of the [NiFe]-hydrogenase from Allochromatium vinosum as studied by stopped-flow infrared spectroscopy. Biochemistry 43:6820–6831

    Article  CAS  PubMed  Google Scholar 

  • Laczkó H (1984) Protective mechanisms in photosynthesis of Anabaena cylindrica. Physiologia Plantarum 63:221–224

    Article  Google Scholar 

  • Laczko I (1986) Appearance of a reversible hydrogenase activity in Anabaena cylindrica grown in high light. Physiologia Plantarum 67:634–637

    Article  CAS  Google Scholar 

  • Lanzilotta WN, Schuller DJ, Thorsteinsson MV et al (2000) Structure of the CO sensing transcription activator CooA. Nat Struct Biol 7:876–80

    Google Scholar 

  • Laurinavichene TV, Rakhely G, Kovacs KL et al (2007) The effect of sulfur compounds on H2 evolution/consumption reactions, mediated by various hydrogenases, in the purple sulfur bacterium, Thiocapsa roseopersicina. Arch Microbiol 188:403–10

    Google Scholar 

  • Lazazzera BA, Beinert H, Khoroshilova N et al (1996) DNA binding and dimerization of the Fe-S-containing FNR protein from Escherichia coli are regulated by oxygen. J Biol Chem 271:2762–2768

    Article  CAS  PubMed  Google Scholar 

  • Leach MR, Sandal S, Sun H et al (2005) Metal binding activity of the Escherichia coli hydrogenase maturation factor HypB. Biochemistry 44:12229–12238

    Article  CAS  PubMed  Google Scholar 

  • Leach MR, Zhang JW, Zamble DB (2007) The role of complex formation between the Escherichia coli hydrogenase accessory factors HypB and SlyD. J Biol Chem 282:16177–16186

    Article  CAS  PubMed  Google Scholar 

  • Leitao E, Oxelfelt F, Oliveira P et al (2005) Analysis of the hupSL operon of the nonheterocystous cyanobacterium Lyngbya majuscula CCAP 1446/4: regulation of transcription and expression under a light-dark regimen. Appl Environ Microbiol 71:4567–4576

    Article  CAS  PubMed  Google Scholar 

  • Lemon BJ, Peters JW (1999) Binding of exogenously added carbon monoxide at the active site of the iron-only hydrogenase (CpI) from Clostridium pasteurianum. Biochemistry 38:12969–12973

    Article  CAS  PubMed  Google Scholar 

  • Lenz O, Bernhard M, Buhrke T et al (2002) The hydrogen-sensing apparatus in Ralstonia eutropha. J Mol Microbiol Biotechnol 4:255–262

    CAS  PubMed  Google Scholar 

  • Lenz O, Friedrich B (1998) A novel multicomponent regulatory system mediates H2 sensing in Alcaligenes eutrophus. Proc Natl Acad Sci USA 95:12474–12479

    Article  CAS  PubMed  Google Scholar 

  • Lenz O, Strack A, Tran-Betcke A et al (1997) A hydrogen-sensing system in transcriptional regulation of hydrogenase gene expression in Alcaligenes species. J Bacteriol 179:1655–1663

    CAS  PubMed  Google Scholar 

  • Lieman-Hurwitz J, Haimovich M, Shalev-Malul G et al (2009) A cyanobacterial AbrB-like protein affects the apparent photosynthetic affinity for CO2 by modulating low-CO2-induced gene expression. Environ Microbiol 11:927–936

    Article  CAS  PubMed  Google Scholar 

  • Lindblad P, Christensson K, Lindberg P et al (2002) Photoproduction of H2 by wildtype Anabaena PCC 7120 and a hydrogen uptake deficient mutant: from laboratory experiments to outdoor culture. Int J Hydrogen Energy:1271–1281

    Google Scholar 

  • Lissolo T, Pulvin S, Thomas D (1984) Reactivation of the hydrogenase from Desulfovibrio gigas by hydrogen. Influence of redox potential. J Biol Chem 259:11725–11729

    CAS  PubMed  Google Scholar 

  • Little JW (1984) Autodigestion of lexA and phage lambda repressors. Proc Natl Acad Sci USA 81:1375–1379

    Article  CAS  PubMed  Google Scholar 

  • Little JW (1991) Mechanism of specific LexA cleavage: autodigestion and the role of RecA coprotease. Biochimie 73:411–421

    Article  CAS  PubMed  Google Scholar 

  • Long M, Liu J, Chen Z et al (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

    Article  CAS  PubMed  Google Scholar 

  • Ludwig M, Cracknell JA, Vincent KA et al (2009) Oxygen-tolerant H2 oxidation by membrane-bound [NiFe] hydrogenases of ralstonia species. Coping with low level H2 in air. J Biol Chem 284:465–477

    Article  CAS  PubMed  Google Scholar 

  • Ludwig M, Schulz-Friedrich R, Appel J (2006) Occurrence of hydrogenases in cyanobacteria and anoxygenic photosynthetic bacteria: implications for the phylogenetic origin of cyanobacterial and algal hydrogenases. J Mol Evol 63:758–768

    Article  CAS  PubMed  Google Scholar 

  • Ma K, Schicho RN, Kelly RM et al (1993) Hydrogenase of the hyperthermophile Pyrococcus furiosus is an elemental sulfur reductase or sulfhydrogenase: evidence for a sulfur-reducing hydrogenase ancestor. Proc Natl Acad Sci USA 90:5341–5344

    Article  CAS  PubMed  Google Scholar 

  • Madigan MT, Ormerod JG (eds) (1995) Taxonomy, physiology and ecology of heliobacteria. Anoxygenic Photosynthetic Bacteria. Kluwer, Dordrecht, The Netherlands

    Google Scholar 

  • Magalon A, Bock A (2000) Analysis of the HypC-hycE complex, a key intermediate in the assembly of the metal center of the Escherichia coli hydrogenase 3. J Biol Chem 275:21114–21120

    Article  CAS  PubMed  Google Scholar 

  • Maier T, Jacobi A, Sauter M et al (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  Google Scholar 

  • Mandin P, Gottesman S (2009) A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol 72:551–565

    Article  CAS  PubMed  Google Scholar 

  • Maness PC, Huang J, Smolinski S et al (2005) Energy generation from the CO oxidation-hydrogen production pathway in Rubrivivax gelatinosus. Appl Environ Microbiol 71:2870–2874

    Article  CAS  PubMed  Google Scholar 

  • Maness PC, Weaver PF (2001) Evidence for three distinct hydrogenase activities in Rhodospirillum rubrum. Appl Microbiol Biotechnol 57:751–756

    Article  CAS  PubMed  Google Scholar 

  • Maroti G, Fodor BD, Rakhely G et al (2003) Accessory proteins functioning selectively and pleiotropically in the biosynthesis of [NiFe] hydrogenases in Thiocapsa roseopersicina. Eur J Biochem 270:2218–2227

    Article  CAS  PubMed  Google Scholar 

  • Martin W, Muller M (1998) The hydrogen hypothesis for the first eukaryote. Nature 392:37–41

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Argudo I, Little R, Shearer N et al (2005) Nitrogen fixation: key genetic regulatory mechanisms. Biochem Soc Trans 33:152–166

    Article  CAS  PubMed  Google Scholar 

  • McGlynn SE, Shepard EM, Winslow MA et al (2008) HydF as a scaffold protein in [FeFe] hydrogenase H-cluster biosynthesis. FEBS Lett 582:2183–2187

    Article  CAS  PubMed  Google Scholar 

  • Menon NK, Robbins J, Wendt JC et al (1991) Mutational analysis and characterization of the Escherichia coli hya operon, which encodes [NiFe] hydrogenase 1. J Bacteriol 173:4851–4861

    CAS  PubMed  Google Scholar 

  • Meyer J (2007) [FeFe] hydrogenases and their evolution: a genomic perspective. Cell Mol Life Sci 64:1063–1084

    Article  CAS  PubMed  Google Scholar 

  • Montet Y, Amara P, Volbeda A et al (1997) Gas access to the active site of Ni-Fe hydrogenases probed by X-ray crystallography and molecular dynamics. Nat Struct Biol 4:523–526

    Article  CAS  PubMed  Google Scholar 

  • Moore LJ, Kiley PJ (2001) Characterization of the dimerization domain in the FNR transcription factor. J Biol Chem 276:45744–45750

    Article  CAS  PubMed  Google Scholar 

  • Muro-Pastor AM, Herrero A, Flores E (2001) Nitrogen-regulated group 2 sigma factor from Synechocystis sp. strain PCC 6803 involved in survival under nitrogen stress. J Bacteriol 183:1090–1095

    Article  CAS  PubMed  Google Scholar 

  • Nakajima H, Aono S (1999) Redox properties of the heme in the CO-sensing transcriptional activator CooA: Electrochemical evidence of the redox-controlled ligand exchange of the heme. Chem Lett 28:1233–1234

    Google Scholar 

  • Nicolet Y, de Lacey AL, Vernede X et al (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

    Article  CAS  PubMed  Google Scholar 

  • Nicolet Y, Piras C, Legrand P et al (1999) Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Structure 7:13–23

    Article  CAS  PubMed  Google Scholar 

  • Nicolet Y, Rubach JK, Posewitz MC et al (2008) X-ray structure of the [FeFe]-hydrogenase maturase HydE from Thermotoga maritima. J Biol Chem 283:18861–18872

    Article  CAS  PubMed  Google Scholar 

  • Novelli PC, Lang PM, Masarie KA et al (1999) Molecular Hydrogen in the troposphere: Global distribution and budget. J Geophys Res 104:30427–30444

    Article  CAS  Google Scholar 

  • Ogata H, Hirota S, Nakahara A et al (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

    Article  CAS  PubMed  Google Scholar 

  • Oliveira P, Leitao E, Tamagnini P et al (2004) Characterization and transcriptional analysis of hupSLW in Gloeothece sp. ATCC 27152: an uptake hydrogenase from a unicellular cyanobacterium. Microbiology 150:3647–3655

    Article  CAS  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

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Olson JW, Maier RJ (2000) Dual roles of Bradyrhizobium japonicum nickel protein in nickel storage and GTP-dependent Ni mobilization. J Bacteriol 182:1702–1705

    Article  CAS  PubMed  Google Scholar 

  • Oren A, Padan E, Avron M (1977) Quantum yields for oxygenic and anoxygenic photosynthesis in the cyanobacterium Oscillatoria limnetica. Proc Natl Acad Sci USA 74:2152–2156

    Article  CAS  PubMed  Google Scholar 

  • Oxelfelt F, Tamagnini P, Salema R et al (1995) Hydrogen uptake in Nostoc strain PCC 73102: effects of nickel, hydrogen, carbon and nitrogen. Plant Physiol. Biochem. 33:617–623

    CAS  Google Scholar 

  • Palacios JM, Murillo J, Leyva A et al (1990) Differential expression of hydrogen uptake (hup) genes in vegetative and symbiotic cells of Rhizobium leguminosarum. Mol Gen Genet 221:363–370

    Article  CAS  PubMed  Google Scholar 

  • Palagyi-Meszaros LS, Maroti J, Latinovics D et al (2009) Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS. Febs J 276:164–174

    Article  CAS  PubMed  Google Scholar 

  • Pandey AS, Harris TV, Giles LJ et al (2008) Dithiomethylether as a ligand in the hydrogenase h-cluster. J Am Chem Soc 130:4533–4540

    Article  CAS  PubMed  Google Scholar 

  • Park KR, Giard JC, Eom JH et al (1999) Cyclic AMP receptor protein and TyrR are required for acid pH and anaerobic induction of hyaB and aniC in Salmonella typhimurium. J Bacteriol 181:689–694

    CAS  PubMed  Google Scholar 

  • Paschos A, Bauer A, Zimmermann A et al (2002) HypF, a carbamoyl phosphate-converting enzyme involved in [NiFe] hydrogenase maturation. J Biol Chem 277:49945–49951

    Article  CAS  PubMed  Google Scholar 

  • Patterson-Fortin LM, Colvin KR, Owttrim GW (2006) A LexA-related protein regulates redox-sensitive expression of the cyanobacterial RNA helicase, crhR. Nucleic Acids Res 34:3446–3454

    Article  CAS  PubMed  Google Scholar 

  • Pedroni P, Della Volpe A, Galli G, Mura GM, Pratesi C, Grandi G (1995) Characterization of the locus encoding the [Ni-Fe] sulfhydrogenase from the archaeon Pyrococcus furiosus: evidence for a relationship to bacterial sulfite reductases. Microbiology 141:449–458

    Article  CAS  PubMed  Google Scholar 

  • Peschek GA (1979) Anaerobic hydrogenase activity in Anacystis nidulans. H2-dependent photoreduction and related reactions. Biochim Biophys Acta 548:187–202

    Article  CAS  PubMed  Google Scholar 

  • Peters JW, Lanzilotta WN, Lemon BJ et al (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282:1853–1858

    Article  CAS  PubMed  Google Scholar 

  • Phillips ZE, Strauch MA (2002) Bacillus subtilis sporulation and stationary phase gene expression. Cell Mol Life Sci 59:392–402

    Article  CAS  PubMed  Google Scholar 

  • Pierik AJ, Roseboom W, Happe RP et al (1999) Carbon monoxide and cyanide as intrinsic ligands to iron in the active site of [NiFe]-hydrogenases. NiFe(CN)2CO, Biology’s way to activate H2. J Biol Chem 274:3331–3337

    Article  CAS  PubMed  Google Scholar 

  • Pierson BK, Castenholz RW (1974) A phototrophic gliding filamentous bacterium of hot springs, Chloroflexus aurantiacus, gen. and sp. nov. Arch Microbiol 100:5–24*

    Article  CAS  PubMed  Google Scholar 

  • Pilet E, Nicolet Y, Mathevon C et al (2009) The role of the maturase HydG in [FeFe]-hydrogenase active site synthesis and assembly. FEBS Lett 583:506–511

    Article  CAS  PubMed  Google Scholar 

  • Posewitz MC, King PW, Smolinski SL et al (2005) Identification of genes required for hydrogenase activity in Chlamydomonas reinhardtii. Biochem Soc Trans 33:102–104

    Article  CAS  PubMed  Google Scholar 

  • Posewitz MC, King PW, Smolinski SL et al (2004) Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J Biol Chem 279:25711–25720

    Article  CAS  PubMed  Google Scholar 

  • Rakhely G, Colbeau A, Garin J et al (1998) Unusual organization of the genes coding for HydSL, the stable [NiFe]hydrogenase in the photosynthetic bacterium Thiocapsa roseopersicina BBS. J Bacteriol 180:1460–1465

    CAS  PubMed  Google Scholar 

  • Rakhely G, Kovacs AT, Maroti G et al (2004) Cyanobacterial-type, heteropentameric, NAD+-reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl Environ Microbiol 70:722–728

    Article  CAS  PubMed  Google Scholar 

  • Rakhely G, Laurinavichene TV, Tsygankov AA et al (2007) The role of Hox hydrogenase in the H2 metabolism of Thiocapsa roseopersicina. Biochim Biophys Acta 1767:671–676

    Article  CAS  PubMed  Google Scholar 

  • Rangarajan ES, Asinas A, Proteau A et al (2008) Structure of [NiFe] hydrogenase maturation protein HypE from Escherichia coli and its interaction with HypF. J Bacteriol 190:1447–1458

    Article  CAS  PubMed  Google Scholar 

  • Rees DC, Akif Tezcan F, Haynes CA et al (2005) Structural basis of biological nitrogen fixation. Philos Transact A Math Phys Eng Sci 363:971–984; discussion 1035–1040

    Article  CAS  PubMed  Google Scholar 

  • Reissmann S, Hochleitner E, Wang H et al (2003) Taming of a poison: biosynthesis of the NiFe-hydrogenase cyanide ligands. Science 299:1067–1070

    Article  CAS  PubMed  Google Scholar 

  • Rey FE, Oda Y, Harwood CS (2006) Regulation of uptake hydrogenase and effects of hydrogen utilization on gene expression in Rhodopseudomonas palustris. J Bacteriol 188:6143–6152

    Article  CAS  PubMed  Google Scholar 

  • Rey L, Fernandez D, Brito B et al (1996) The hydrogenase gene cluster of Rhizobium leguminosarum bv. viciae contains an additional gene ( hypX), which encodes a protein with sequence similarity to the N10-formyltetrahydrofolate-dependent enzyme family and is required for nickel-dependent hydrogenase processing and activity. Mol Gen Genet 252:237–248

    CAS  PubMed  Google Scholar 

  • Richard DJ, Sawers G, Sargent F et al (1999) Transcriptional regulation in response to oxygen and nitrate of the operons encoding the [NiFe] hydrogenases 1 and 2 of Escherichia coli. Microbiology 145 (Pt 10): 2903–2912

    CAS  PubMed  Google Scholar 

  • Roberts GP, Kerby RL, Youn H et al (2005) CooA, a paradigm for gas sensing regulatory proteins. J Inorg Biochem 99:280–292

    Article  CAS  PubMed  Google Scholar 

  • Rosano C, Zuccotti S, Bucciantini M et al (2002) Crystal structure and anion binding in the prokaryotic hydrogenase maturation factor HypF acylphosphatase-like domain. J Mol Biol 321:785–796

    Article  CAS  PubMed  Google Scholar 

  • Roseboom W, Blokesch M, Bock A et al (2005) The biosynthetic routes for carbon monoxide and cyanide in the Ni-Fe active site of hydrogenases are different. FEBS Lett 579:469–472

    Article  CAS  PubMed  Google Scholar 

  • Rossmann R, Maier T, Lottspeich F et al (1995) Characterisation of a protease from Escherichia coli involved in hydrogenase maturation. Eur J Biochem 227:545–550

    Article  CAS  PubMed  Google Scholar 

  • Rubach JK, Brazzolotto X, Gaillard J et al (2005) Biochemical characterization of the HydE and HydG iron-only hydrogenase maturation enzymes from Thermatoga maritima. FEBS Lett 579:5055–5060

    Article  CAS  PubMed  Google Scholar 

  • Sandman K, Pereira SL, Reeve JN (1998) Diversity of prokaryotic chromosomal proteins and the origin of the nucleosome. Cell Mol Life Sci 54:1350–1364

    Article  CAS  PubMed  Google Scholar 

  • Sapra R, Verhagen MF, Adams MW (2000) Purification and characterization of a membrane-bound hydrogenase from the hyperthermophilic archaeon Pyrococcus furiosus. J Bacteriol 182:3423–3428

    Article  CAS  PubMed  Google Scholar 

  • Sattley WM, Madigan MT, Swingley WD et al (2008) The genome of Heliobacterium modesticaldum, a phototrophic representative of the Firmicutes containing the simplest photosynthetic apparatus. J Bacteriol 190:4687–4696

    Article  CAS  PubMed  Google Scholar 

  • Sauter M, Bohm R, Bock A (1992) Mutational analysis of the operon ( hyc) determining hydrogenase 3 formation in Escherichia coli. Mol Microbiol 6:1523–1532

    Article  CAS  PubMed  Google Scholar 

  • Sawers G, Heider J, Zehelein E et al (1991) Expression and operon structure of the sel genes of Escherichia coli and identification of a third selenium-containing formate dehydrogenase isoenzyme. J Bacteriol 173:4983–4993

    CAS  PubMed  Google Scholar 

  • Sawers RG, Blokesch, M Böck, A (2004) Anaerobic formate and hydrogen metabolism. EcoSal- Escherichia coli and Salmonella: Cellular and Molecular Biology. R. Curtiss III E. i. C. Washington, DC, ASM Press

    Google Scholar 

  • Schmitz O, Boison G, Bothe H (2001) Quantitative analysis of expression of two circadian clock-controlled gene clusters coding for the bidirectional hydrogenase in the cyanobacterium Synechococcus sp. PCC7942. Mol Microbiol 41:1409–1417

    Article  CAS  PubMed  Google Scholar 

  • Schmitz O, Boison G, Salzmann H et al (2002) HoxE–a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. Biochim Biophys Acta 1554:66–74

    Article  CAS  PubMed  Google Scholar 

  • Schneider K, Schlegel HG (1976) Purification and properties of soluble hydrogenase from Alcaligenes eutrophus H 16. Biochim Biophys Acta 452:66–80

    Article  CAS  PubMed  Google Scholar 

  • Schultz JE, Weaver PF (1982) Fermentation and anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata. J Bacteriol 149:181–190

    CAS  PubMed  Google Scholar 

  • Schut GJ, Adams MW (2009) The iron-hydrogenase of Thermotoga maritima utilizes ferredoxin and NADH synergistically: a new perspective on anaerobic hydrogen production. J Bacteriol 191:4451–4457

    Article  CAS  PubMed  Google Scholar 

  • Schwartz CJ, Djaman O, Imlay JA et al (2000) The cysteine desulfurase, IscS, has a major role in in vivo Fe-S cluster formation in Escherichia coli. Proc Natl Acad Sci USA 97:9009–9014

    Article  CAS  PubMed  Google Scholar 

  • Schwartz E, Friedrich B (2006) The H2-metabolizing prokaryotes. The prokaryotes. In: Dworkin M, Falkow S, Rosenberg E, Schleifer KH, Stackebrandt E (eds) A handbook on the biology of bacteria. New York, Springer

    Google Scholar 

  • Self WT, Grunden AM, Hasona A et al (1999) Transcriptional regulation of molybdoenzyme synthesis in Escherichia coli in response to molybdenum: ModE-molybdate, a repressor of the modABCD (molybdate transport) operon is a secondary transcriptional activator for the hyc and nar operons. Microbiology 145(Pt 1): 41–55

    Article  CAS  PubMed  Google Scholar 

  • Serebryakova L, Zorin N, Lindblad P (1994) Reversible hydrogenase in Anabaena variabilis ATCC 29413. Presence and localization in non-N2-fixing cells. Arch Microbiol 161:140–144

    Google Scholar 

  • Serebryakova LT, Medina M, Zorin NA et al (1996) Reversible hydrogenase of Anabaena variabilis ATCC 29413: catalytic properties and characterization of redox centres. FEBS Lett 383:79–82

    Article  CAS  PubMed  Google Scholar 

  • Serebryakova LT, Sheremetieva M, Tsygankov AA (1998) Reversible hydrogenase activity of Gloeocapsa alpicola in continuous culture. FEMS Microbiology Letters 166:89–94

    Article  CAS  Google Scholar 

  • Serebryakova LT, Zorin NA, Gogotov IN (1992) Hydrogenase activity in filamentous cyanobacteria. Mikrobiologiya 61:107–112

    Google Scholar 

  • Severin I, Stal LJ (2008) Light dependency of nitrogen fixation in a coastal cyanobacterial mat. ISME J 2:1077–1088

    Article  CAS  PubMed  Google Scholar 

  • Shalev-Malul G, Lieman-Hurwitz J, Viner-Mozzini Y et al (2008) An AbrB-like protein might be involved in the regulation of cylindrospermopsin production by Aphanizomenon ovalisporum. Environ Microbiol 10:988–999

    Article  CAS  PubMed  Google Scholar 

  • Shelver D, Kerby RL, He Y et al (1997) CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein. Proc Natl Acad Sci USA 94:11216–11220

    Article  CAS  PubMed  Google Scholar 

  • Shomura Y, Komori H, Miyabe N et al (2007) Crystal structures of hydrogenase maturation protein HypE in the Apo and ATP-bound forms. J Mol Biol 372:1045–1054

    Article  CAS  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

    Article  PubMed  CAS  Google Scholar 

  • Skibinski DA, Golby P, Chang YS et al (2002) Regulation of the hydrogenase-4 operon of Escherichia coli by the sigma(54)-dependent transcriptional activators FhlA and HyfR. J Bacteriol 184:6642–6653

    Article  CAS  PubMed  Google Scholar 

  • Stal LJ, Moezelaar R (1997) Fermentation in cyanobacteria. FEMS microbiology reviews 21:179–211

    Article  CAS  Google Scholar 

  • Stensjo K, Ow SY, Barrios-Llerena ME et al (2007) An iTRAQ-based quantitative analysis to elaborate the proteomic response of Nostoc sp. PCC 7120 under N2 fixing conditions. J Proteome Res 6:621–635

    Article  PubMed  CAS  Google Scholar 

  • Stephenson M, Stickland LH (1931) Hydrogenase: a bacterial enzyme activating molecular hydrogen: The properties of the enzyme. Biochem J 25:205–214

    CAS  PubMed  Google Scholar 

  • Summerfield TC, Sherman LA (2008) Global transcriptional response of the alkali-tolerant cyanobacterium Synechocystis sp. strain PCC 6803 to a pH 10 environment. Appl Environ Microbiol 74:5276–5284

    Article  CAS  PubMed  Google Scholar 

  • Svetlitchnyi V, Peschel C, Acker G et al (2001) Two membrane-associated NiFeS-carbon monoxide dehydrogenases from the anaerobic carbon-monoxide-utilizing eubacterium Carboxydothermus hydrogenoformans. J Bacteriol 183:5134–5144

    Article  CAS  PubMed  Google Scholar 

  • Swem LR, Elsen S, Bird TH et al (2001) The RegB/RegA two-component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus. J Mol Biol 309:121–138

    Article  CAS  PubMed  Google Scholar 

  • Swem LR, Gong X, Yu CA et al (2006) Identification of a ubiquinone-binding site that affects autophosphorylation of the sensor kinase RegB. J Biol Chem 281:6768–6775

    Article  CAS  PubMed  Google Scholar 

  • Swem LR, Kraft BJ, Swem DL et al (2003) Signal transduction by the global regulator RegB is mediated by a redox-active cysteine. EMBO J 22:4699–4708

    Article  CAS  PubMed  Google Scholar 

  • Tamagnini P, Leitao E, Oliveira P et al (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol Rev 31:692–720

    Article  CAS  PubMed  Google Scholar 

  • Tel-Or E, Luijk LW, Packer L (1977) An inducible hydrogenase in cyanobacteria enhances N2 fixation. FEBS Lett 78:49–52

    Article  CAS  PubMed  Google Scholar 

  • Thauer RK, Jungermann K, Decker K (1977) Energy conservation in chemotrophic anaerobic bacteria. Bacteriol Rev 41:100–180

    CAS  PubMed  Google Scholar 

  • Theodoratou E, Huber R, Bock A (2005) [NiFe]-Hydrogenase maturation endopeptidase: structure and function. Biochem Soc Trans 33:108–111

    Article  CAS  PubMed  Google Scholar 

  • Theodoratou E, Paschos A, Magalon A et al (2000) Nickel serves as a substrate recognition motif for the endopeptidase involved in hydrogenase maturation. Eur J Biochem 267:1995–1999

    Article  CAS  PubMed  Google Scholar 

  • Toepel J, Welsh E, Summerfield T et al (2008) Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J Bacteriol 190:3904–3913

    Article  CAS  PubMed  Google Scholar 

  • Toussaint B, Bosc C, Richaud P et al (1991) A mutation in a Rhodobacter capsulatus gene encoding an integration host factor-like protein impairs in vivo hydrogenase expression. Proc Natl Acad Sci USA 88:10749–10753

    Article  CAS  PubMed  Google Scholar 

  • Toussaint B, de Sury d’Aspremont R, Delic-Attree I et al (1997) The Rhodobacter capsulatus hupSLC promoter: identification of cis-regulatory elements and of trans-activating factors involved in H2 activation of hupSLC transcription. Mol Microbiol 26:927–937

    Article  CAS  PubMed  Google Scholar 

  • Troshina O, Serebryakova L,Sheremetieva M et al (2002) Production of H2 by the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 during fermentation. Int J Hydrogen Energy 27:1283–1289

    Article  CAS  Google Scholar 

  • Van Bruggen JJA, Stumm CK, Vogels GD (1983) Symbiosis of methanogenic bacteria and sapropelic protozoa. Arch Microbiol J 36:89–95

    Article  Google Scholar 

  • Van der Linden E, Burgdorf T, Bernhard M et al (2004) The soluble [NiFe]-hydrogenase from Ralstonia eutropha contains four cyanides in its active site, one of which is responsible for the insensitivity towards oxygen. J Biol Inorg Chem 9:616–626

    Article  PubMed  CAS  Google Scholar 

  • Van der Oost J, Cox RP (1988) Hydrogenase activity in nitrate-grown cells of the unicellular cyanobacterium Cyanothece PCC 7822. Arch of Microbiol 151:40–43

    Article  Google Scholar 

  • Van der Zwaan JW, Coremans JM, Bouwens EC et al (1990) Effect of17O2 and13CO on EPR spectra of nickel in hydrogenase from Chromatium vinosum. Biochim. Biophys. Acta 1041:101–110

    Article  PubMed  Google Scholar 

  • Van Praag E, Degli Agosti R, Bachofen R (2000) Rhythmic activity of uptake hydrogenase in the prokaryote Rhodospirillum rubrum. J Biol Rhythms 15:218–224

    Article  PubMed  Google Scholar 

  • Vaughn JL, Feher V, Naylor S et al (2000) Novel DNA binding domain and genetic regulation model of Bacillus subtilis transition state regulator abrB. Nat Struct Biol 7:1139–1146

    Article  CAS  PubMed  Google Scholar 

  • Vignais PM (2008) Hydrogenases and H(+)-reduction in primary energy conservation. Results Probl Cell Differ 45:223–252

    Article  CAS  PubMed  Google Scholar 

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

    Article  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 

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

    CAS  PubMed  Google Scholar 

  • Vignais PM, Elsen S, Colbeau A (2005) Transcriptional regulation of the uptake [NiFe]hydrogenase genes in Rhodobacter capsulatus. Biochem Soc Trans 33:28–32

    Article  CAS  PubMed  Google Scholar 

  • Vignais PM, Toussaint B (1994) Molecular biology of membrane-bound H2 uptake hydrogenases. Arch Microbiol 161:1–10

    CAS  PubMed  Google Scholar 

  • Volbeda A, Charon MH, Piras C et al (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373:580–587

    Article  CAS  PubMed  Google Scholar 

  • Volbeda A, Fontecilla-Camps JC, Frey M (1996) Novel metal sites in protein structures. Curr Opin Struct Biol 6:804–812

    Article  CAS  PubMed  Google Scholar 

  • Volbeda A, Martin L, Cavazza C et al (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J Biol Inorg Chem 10:239–249

    Article  CAS  PubMed  Google Scholar 

  • Watanabe S, Arai T, Matsumi R et al (2009) Crystal Structure of HypA, a Nickel-Binding Metallochaperone for [NiFe] Hydrogenase Maturation. J Mol Biol 394:448–459

    Google Scholar 

  • Watanabe S, Matsumi R, Arai T et al (2007) Crystal structures of [NiFe] hydrogenase maturation proteins HypC, HypD, and HypE: insights into cyanation reaction by thiol redox signaling. Mol Cell 27:29–40

    Article  CAS  PubMed  Google Scholar 

  • Waugh R, Boxer DH (1986) Pleiotropic hydrogenase mutants of Escherichia coli K12: growth in the presence of nickel can restore hydrogenase activity. Biochimie 68:157–166

    Article  CAS  PubMed  Google Scholar 

  • Weyman PD, Pratte B, Thiel T (2008) Transcription of hupSL in Anabaena variabilis ATCC 29413 is regulated by NtcA and not by hydrogen. Appl Environ Microbiol 74:2103–2110

    Article  CAS  PubMed  Google Scholar 

  • Wu J, Bauer CE (2008) RegB/RegA, a global redox-responding two-component system. Adv Exp Med Biol 631:131–148

    Article  CAS  PubMed  Google Scholar 

  • Xu K, Strauch MA (1996) In vitro selection of optimal AbrB-binding sites: comparison to known in vivo sites indicates flexibility in AbrB binding and recognition of three-dimensional DNA structures. Mol Microbiol 19:145–158

    Article  CAS  PubMed  Google Scholar 

  • Yang F, Hu W, Xu H et al (2007) Solution structure and backbone dynamics of an endopeptidase HycI from Escherichia coli: implications for mechanism of the [NiFe] hydrogenase maturation. J Biol Chem 282:3856–3863

    Article  CAS  PubMed  Google Scholar 

  • Zannoni D (1995) In: Blankenship RE, Miller M, Bauer CE (eds) Anoxygenic Photosynthetic Bacteria.. Kluwer Academic, Dordrecht pp. 949–971

    Google Scholar 

  • Zhang JW, Butland G, Greenblatt JF et al (2005) A role for SlyD in the Escherichia coli hydrogenase biosynthetic pathway. J Biol Chem 280:4360–4366

    Article  CAS  PubMed  Google Scholar 

  • Zhang Z, Pendse ND, Phillips KN et al (2008) Gene expression patterns of sulfur starvation in Synechocystis sp. PCC 6803. BMC Genomics 9:344

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Life Science, Arizona State University, 874501, Tempe, AZ, 85287, USA

    Christoph Schwarz, Zach Poss, Doerte Hoffmann & Jens Appel

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  1. Christoph Schwarz
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  2. Zach Poss
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Correspondence to Christoph Schwarz .

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  1. Dépt. de microbiologie et immunologie, Université de Montréal, Montreal, H3C 3J7, Canada

    Patrick C. Hallenbeck

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Schwarz, C., Poss, Z., Hoffmann, D., Appel, J. (2010). Hydrogenases and Hydrogen Metabolism in Photosynthetic Prokaryotes. In: Hallenbeck, P. (eds) Recent Advances in Phototrophic Prokaryotes. Advances in Experimental Medicine and Biology, vol 675. Springer, New York, NY. https://doi.org/10.1007/978-1-4419-1528-3_18

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