[NiFe] Group 1b-hydrogenase

This entry was last updated at: Feb. 9, 2018, 7:09 a.m.

Properties

Group	[NiFe] Group 1: Respiratory H₂-uptake [NiFe] hydrogenases
Subgroup	[NiFe] Group 1b: Prototypical
Function	Hydrogenotrophic respiration using sulfate, fumarate, nitrate, metals, and azo compounds as terminal electron acceptors. Enzyme transfers H₂-liberated electrons through cytochromes to terminal reductase.
Activity	H₂-uptake (unidirectional)
Oxygen tolerance	O₂-sensitive
Localisation	Membrane-bound or periplasmic

Distribution

Ecosystem distribution	Anoxic soils and sediments, marine waters, animal gastrointestinal tracts
Taxonomic distribution	Widespread in Deltaproteobacteria and Epsilonproteobacteria

Genetic Organisation

e.g. Wolinella succinogenes (WP_011139497.1):

Architecture

Structures	4U9H (Desulfovibrio vulgaris, 0.9 Å resolution, reduced) 4U9I (Desulfovibrio vulgaris, 1.1 Å resolution, reduced) 1H2R (Desulfovibrio vulgaris, 1.4 Å resolution, active) 1H2A (Desulfovibrio vulgaris, 1.8 Å resolution, oxidised) 1YRQ (Desulfovibrio fructosovorans, 2.1 Å resolution, oxidised) 4URH (Desulfovibrio fructosovorans, 1.4 Å resolution, oxidised) 1YQW (Desulfovibrio fructosovorans, 1.8 Å resolution, oxidised) 4FRF (Desulfovibrio fructosovorans, 2.7 Å resolution, oxidised) 1YQ9 (Desulfovibrio gigas, 2.4 Å resolution, oxidised) 2FRV (Desulfovibrio gigas, 2.5 Å resolution, oxidised) 1FRV (Desulfovibrio gigas, 2.9 Å resolution, oxidised) 1E3D (Desulfovibrio desulfuricans, 1.8 Å resolution, oxidised)
Subunits	3
Subunit description	HynB (hydrogenase large subunit) HynA (hydrogenase small subunit) HynC (cytochrome b subunit) In Deltaproteobacteria, CycA (cytochrome c₃ subunit) substitutes for HynC
Catalytic site	[NiFe]-centre
FeS clusters	Proximal: 4Cys[4Fe4S] or 3Cys1Asn[4Fe4S] Medial: 3Cys[3Fe4S] Distal: 3Cys1His[4Fe4S]

Sequences in this class

NCBI Accession	Organism	Hydrogenase Class	Phylum	Order	Activity (Predicted)	Oxygen Tolerance (Predicted)	Subunits (Predicted)	Metal Centres (Predicted)	Accessory Subunits (Predicted)
WP_013344606.1	Ferrimonas balearica	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028110915.1	Ferrimonas futtsuensis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028112170.1	Ferrimonas kyonanensis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028115083.1	Ferrimonas senticii	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011759792.1	Shewanella amazonensis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_014620707.1	Shewanella baltica	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028762126.1	Shewanella colwelliana	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_023267287.1	Shewanella decolorationis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028768898.1	Shewanella fidelis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011637560.1	Shewanella frigidimarina	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_012277350.1	Shewanella halifaxensis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011865562.1	Shewanella loihica	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011072162.1	Shewanella oneidensis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_012155268.1	Shewanella pealeana	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_020912731.1	Shewanella piezotolerans	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028760177.1	Shewanella putrefaciens	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_012142253.1	Shewanella sediminis	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011622592.1	Shewanella sp. MR-4	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_028774221.1	Shewanella waksmanii	[NiFe] Group 1b	Gammaproteobacteria	Alteromonadales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011371454.1	Thiomicrospira crunogena	[NiFe] Group 1b	Gammaproteobacteria	Thiotrichales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_005368230.1	Photobacterium angustum	[NiFe] Group 1b	Gammaproteobacteria	Vibrionales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_005299657.1	Photobacterium damselae	[NiFe] Group 1b	Gammaproteobacteria	Vibrionales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_008987220.1	Photobacterium leiognathi	[NiFe] Group 1b	Gammaproteobacteria	Vibrionales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_023403981.1	Vibrio halioticoli	[NiFe] Group 1b	Gammaproteobacteria	Vibrionales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_014353799.1	Sulfobacillus acidophilus	[NiFe] Group 1b	Firmicutes	Clostridiales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_020374232.1	Sulfobacillus thermosulfidooxidans	[NiFe] Group 1b	Firmicutes	Clostridiales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_014468932.1	Arcobacter butzleri	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_014468937.1	Arcobacter butzleri	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_013135169.1	Arcobacter nitrofigilis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_013135164.1	Arcobacter nitrofigilis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_020975057.1	Campylobacter coli	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_021091366.1	Campylobacter concisus	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_027305891.1	Campylobacter cuniculorum	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_018136329.1	Campylobacter curvus	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_002849472.1	Campylobacter fetus	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_005870439.1	Campylobacter gracilis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_012108717.1	Campylobacter hominis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_002869087.1	Campylobacter jejuni	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_012661425.1	Campylobacter lari	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_002952687.1	Campylobacter showae	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_004277637.1	Campylobacter upsaliensis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_016647003.1	Campylobacter ureolyticus	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_011577655.1	Helicobacter acinonychis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_004087140.1	Helicobacter bilis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_013890446.1	Helicobacter bizzozeronii	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_006655925.1	Helicobacter canadensis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_023929963.1	Helicobacter canis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_014661358.1	Helicobacter cetorum	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_002956442.1	Helicobacter cinaedi	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome
WP_013469730.1	Helicobacter felis	[NiFe] Group 1b	Epsilonproteobacteria	Campylobacterales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 2 x [4Fe4S] clusters, 1 x [3Fe4S] cluster	Cytochrome

Literature

Genetics:

Deckers, H.M., Wilson, F.R., and Voordouw, G. (1990) Cloning and sequencing of a [NiFe] hydrogenase operon from Desulfovibrio vulgaris Miyazaki F. Microbiol. 136: 2021-2028.
Greening, C., Biswas, A., Carere, C.R., Jackson, C.J., Taylor, M.C., Stott, M.B., Cook, G.M., and Morales, S.E. (2016) Genomic and metagenomic surveys of hydrogenase distribution indicate H₂ is a widely utilised energy source for microbial growth and survival. ISME J. 10: 761-777.
Kruse, S., Goris, T., Wolf, M., Wei, X., and Diekert, G. (2017). The NiFe hydrogenases of the tetrachloroethene-respiring Epsilonproteobacterium Sulfurospirillum multivorans: biochemical studies and transcription analysis. Front. Microbiol. 8: 444.
Li, C., Peck Jr, H.D., LeGall, J., and Przybyla, A.E. (1987) Cloning, characterization, and sequencing of the genes encoding the large and small subunits of the periplasmic [NiFe] hydrogenase of Desulfovibrio gigas. DNA 6: 539-551.
Rousset, M., Dermoun, Z., Chippaux, M., and Belaich, J.P. (1991) Marker exchange mutagenesis of the hydN genes in Desulfovibrio fructosovorans. Mol. Microbiol. 5: 1735-1740.
Rousset, M., Dermoun, Z., Hatchikian, C.E., and Bélaich, J.P. (1990) Cloning and sequencing of the locus encoding the large and small subunit genes of the periplasmic [NiFe] hydrogenase from Desulfovibrio fructosovorans. Gene 94: 95-101.
Rousset, M., Dermoun, Z., Wall, J.D., and Belaich, J.P. (1993) Analysis of the periplasmic [NiFe] hydrogenase transcription unit from Desulfovibrio fructosovorans. J. Bacteriol. 175: 3388-3393.
Rousset, M., Magro, V., Forget, N., Guigliarelli, B., Belaich, J.P., and Hatchikian, E.C. (1998) Heterologous expression of the Desulfovibrio gigas [NiFe] hydrogenase in Desulfovibrio fructosovorans MR400. J. Bacteriol. 180: 4982-4986.
Voordouw, G. and Brenner, S. (1985) Nucleotide sequence of the gene encoding the hydrogenase from Desulfovibrio vulgaris (Hildenborough). Eur. J. Biochem. 148: 515-520.
Voordouw, G., Menon, N.K., LeGall, J., Choi, E.S., Peck, H.D., and Przybyla, A.E. (1989) Analysis and comparison of nucleotide sequences encoding the genes for [NiFe] and [NiFeSe] hydrogenases from Desulfovibrio gigas and Desulfovibrio baculatus. J. Bacteriol. 171: 2894-2899.
van der Stel, A.X., Boogerd, F.C., Huynh, S., Parker, C.T., van Dijk, L., van Putten, J.P. and Wösten, M.M. (2017) Generation of the membrane potential and its impact on the motility, ATP production and growth in Campylobacter jejuni. Mol. Microbiol. 105: 637-651.
Voordouw, G., Niviere, V., Ferris, F.G., Fedorak, P.M., and Westlake, D.W. (1990) Distribution of hydrogenase genes in Desulfovibrio spp. and their use in identification of species from the oil field environment. Appl. Environ. Microbiol. 56: 3748-3754.
Wawer, C., Jetten, M.S., and Muyzer, G. (1997) Genetic diversity and expression of the [NiFe] hydrogenase large-subunit gene of Desulfovibrio spp. in environmental samples. Appl. Environ. Microbiol. 63: 4360-4369.

Physiology:

Badziong, W., Thauer, R.K., and Zeikus, J.G. (1978) Isolation and characterization of Desulfovibrio growing on hydrogen plus sulfate as the sole energy source. Arch. Microbiol. 116: 41-49.
Bell, G.R., LeGall, J., and Peck, H.D. (1974) Evidence for the periplasmic location of hydrogenase in Desulfovibrio gigas. J. Bacteriol. 120: 994-997.
Brandis, A. and Thauer, R.K. (1981) Growth of Desulfovibrio species on hydrogen and sulphate as sole energy source. Microbiol. 126: 249-252.
Caffrey, S.M., Park, H.S., Voordouw, J.K., He, Z., Zhou, J., and Voordouw, G. (2007) Function of periplasmic hydrogenases in the sulfate-reducing bacterium Desulfovibrio vulgaris Hildenborough. J. Bacteriol. 189: 6159-6167.
Casalot, L., Valette, O., De Luca, G., Dermoun, Z., Rousset, M., and de Philip, P., (2002) Construction and physiological studies of hydrogenase depleted mutants of Desulfovibrio fructosovorans. FEMS Microbiol. Lett. 214: 107-112.
Chardin, B., Giudici-Orticoni, M.T., De Luca, G., Guigliarelli, B. and Bruschi, M. (2003) Hydrogenases in sulfate-reducing bacteria function as chromium reductase. Appl. Microbiol. Biotechnol. 63: 315-321.
Da Silva, S.M., Venceslau, S.S., Fernandes, C.L., Valente, F.M., and Pereira, I.A,. (2008) Hydrogen as an energy source for the human pathogen Bilophila wadsworthia. Antonie Van Leeuwenhoek 93: 381-390.
De Luca, G., de Philip, P., Dermoun, Z., Rousset, M., and Verméglio, A. (2001) Reduction of technetium(VII) by Desulfovibrio fructosovorans is mediated by the nickel-iron hydrogenase. Appl. Environ. Microbiol. 67: 4583-4587.
Dolla, A., Pohorelic, B.K., Voordouw, J.K., and Voordouw, G. (2000) Deletion of the hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough hampers hydrogen metabolism and low-redox-potential niche establishment. Arch. Microbiol. 174: 143-151.
Dross, F., Geisler, V., Lenger, R., Theis, F., Krafft, T., Fahrenholz, F., Kojro, E., Duchêne, A. Tripier, D., Juvenal, K. and Kröger, A. (1992) The quinone-reactive Ni/Fe-hydrogenase of Wolinella succinogenes. Eur. J. Biochem. 206: 93-102.
Goodman, T.G. and Hoffman, P.S. (1983) Hydrogenase activity in catalase-positive strains of Campylobacter spp. J. Clin. Microbiol. 18: 825-829.
Gross, R., Simon, J., Theis, F., and Kröger, A. (1998) Two membrane anchors of Wolinella succinogenes hydrogenase and their function in fumarate and polysulfide respiration. Arch. Microbiol. 170: 50-58.
Hamann, E. et al. (2016) Environmental Breviatea harbour mutualistic Arcobacter epibionts. Nature 534: 254-258.
Hansen, M. and Perner, M. (2015) A novel hydrogen oxidizer amidst the sulfur-oxidizing Thiomicrospira lineage. ISME J. 9: 696-707.
Howlett, R.M., Hughes, B.M., Hitchcock, A. and Kelly, D.J. (2012) Hydrogenase activity in the foodborne pathogen Campylobacter jejuni depends upon a novel ABC-type nickel transporter (NikZYXWV) and is SlyD-independent. Microbiol. 158: 1645-1655.
Jankielewicz, A., Klimmek, O., and Kröger, A. (1995) The electron transfer from hydrogenase and formate dehydrogenase to polysulfide reductase in the membrane of Wolinella succinogenes. BBA Bioenerg. 1231: 157-162.
Kuhns, L.G., Benoit, S.L., Bayyareddy, K., Johnson, D., Orlando, R., Evans, A.L., Waldrop, G.L., and Maier, R.J. (2016) Carbon fixation driven by molecular hydrogen results in chemolithoautotrophically enhanced growth of Helicobacter pylori. J. Bacteriol. 198: 1423-1428.
Le Laz, S., Kpebe, A., Lorquin, J., Brugna, M. and Rousset, M. (2014) H₂-dependent azoreduction by Shewanella oneidensis MR-1: involvement of secreted flavins and both [Ni-Fe] and [Fe-Fe] hydrogenases. Appl. Microbiol. Biotechnol. 98: 2699-2707.
Li, X., McInerney, M.J., Stahl, D.A. and Krumholz, L.R., 2011. Metabolism of H₂ by Desulfovibrio alaskensis G20 during syntrophic growth on lactate. Microbiol. 157: 2912-2921.
Maier, R.J., Fu, C., Gilbert, J., Moshiri, F., Olson, J., and Plaut, A.G. (1996) Hydrogen uptake hydrogenase in Helicobacter pylori. FEMS Microbiol. Lett. 141: 71-76.
Maier, R.J., Olson, J., and Olczak, A. (2003) Hydrogen-oxidizing capabilities of Helicobacter hepaticus and in vivo availability of the substrate. J. Bacteriol. 185: 2680-2682.
Malki, S., De Luca, G., Fardeau, M.L., Rousset, M., Belaich, J.P., and Dermoun, Z. (1997) Physiological characteristics and growth behavior of single and double hydrogenase mutants of Desulfovibrio fructosovorans. Arch. Microbiol. 167: 38-45.
Marshall, M.J. et al. (2008) Hydrogenase-and outer membrane c-type cytochrome-facilitated reduction of technetium(VII) by Shewanella oneidensis MR-1. Environ. Microbiol. 10: 125-136.
Mehta, N.S., Benoit, S., Mysore, J.V., Sousa, R.S., and Maier, R.J. (2005) Helicobacter hepaticus hydrogenase mutants are deficient in hydrogen-supported amino acid uptake and in causing liver lesions in A/J mice. Infect. Immun. 73: 5311-5318.
Meshulam-Simon, G., Behrens, S., Choo, A.D., and Spormann, A.M. (2007) Hydrogen metabolism in Shewanella oneidensis MR-1. Appl. Environ. Microbiol. 73: 1153-1165.
Meyer, B., Kuehl, J.V., Deutschbauer, A.M., Arkin, A.P., and Stahl, D.A. (2013) Flexibility of syntrophic enzyme systems in Desulfovibrio species ensures their adaptation capability to environmental changes. J. Bacteriol. 195: 4900-4914.
Morais-Silva, F.O., Santos, C.I., Rodrigues, R., Pereira, I.A., and Rodrigues-Pousada, C. (2013) Roles of HynAB and Ech, the only two hydrogenases found in the model sulfate reducer Desulfovibrio gigas. J. Bacteriol. 195: 4753-4760.
Olson, J.W. and Maier, R.J. (2002) Molecular hydrogen as an energy source for Helicobacter pylori. Science 298: 1788-1790.
Pereira, I.A., Romão, C.V., Xavier, A.V., LeGall, J., and Teixeira, M. (1998) Electron transfer between hydrogenases and mono-and multiheme cytochromes in Desulfovibrio ssp. J. Biol. Inorg. Chem. 3 494-498.
Rapp-Giles, B.J., Casalot, L., English, R.S., Ringbauer, J.A., Dolla, A., and Wall, J.D. (2000) Cytochrome c₃ mutants of Desulfovibrio desulfuricans. Appl. Environ. Microbiol. 66: 671-677.
Schumacher, W., Kroneck, P.M., and Pfennig, N. (1992) Comparative systematic study on "Spirillum" 5175, Campylobacter and Wolinella species. Arch. Microbiol. 158: 287-293.
Wang, G., Romero-Gallo, J., Benoit, S.L., Piazuelo, M.B., Dominguez, R.L., Morgan, D.R., Peek, R.M., and Maier, R.J. (2016) Hydrogen metabolism in Helicobacter pylori plays a role in gastric carcinogenesis through facilitating CagA translocation. mBio 7: e01022-16.
Weerakoon, D.R., Borden, N.J., Goodson, C.M., Grimes, J., and Olson, J.W. (2009) The role of respiratory donor enzymes in Campylobacter jejuni host colonization and physiology. Microb. Pathog. 47: 8-15.

Biochemistry:

Berlier, Y., Fauque, G.D., LeGall, J., Choi, E.S., Peck, H.D. and Lespinat, P.A. (1987) Inhibition studies of three classes of Desulfovibrio hydrogenase: application to the further characterization of the multiple hydrogenases found in Desulfovibrio vulgaris Hildenborough. Biochem. Biophys. Res. Commun. 146: 147-153.
Dementin, S., Burlat, B., De Lacey, A.L., Pardo, A., Adryanczyk-Perrier, G., Guigliarelli, B., Fernandez, V.M., and Rousset, M. (2004) A glutamate is the essential proton transfer gate during the catalytic cycle of the [NiFe] hydrogenase. J. Biol. Chem. 279: 10508-10513.
Fernandez, V.M., Hatchikian, E.C., and Cammack, R. (1985) Properties and reactivation of two different deactivated forms of Desulfovibrio gigas hydrogenase. BBA Prot. Struct. Mol. Enzymol. 832: 69-79.
Gross, R., Simon, J., Lancaster, C.R.D., and Kröger, A. (1998) Identification of histidine residues in Wolinella succinogenes hydrogenase that are essential for menaquinone reduction by H₂. Mol. Microbiol. 30: 639-646.
Gross, R., Pisa, R., Sänger, M., Lancaster, C.R.D., and Simon, J. (2004) Characterization of the menaquinone reduction site in the diheme cytochrome b membrane anchor of Wolinella succinogenes NiFe-hydrogenase. J. Biol. Chem. 279: 274-281.
Hatchikian, C.E., Traore, A.S., Fernandez, V.M., and Cammack, R. (1990) Characterization of the nickel-iron periplasmic hydrogenase from Desulfovibrio fructosovorans. Eur. J. Biochem. 187: 635-643.
Higuchi, Y., Ogata, H., Miki, K., Yasuoka, N., and Yagi, T. (1999) Removal of the bridging ligand atom at the Ni-Fe active site of [NiFe] hydrogenase upon reduction with H₂, as revealed by X-ray structure analysis at 1.4 Å resolution. Structure 7: 549-556.
Higuchi, Y., Yagi, T., and 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.
Leroux, F., Dementin, S., Burlat, B., Cournac, L., Volbeda, A., Champ, S., Martin, L., Guigliarelli, B., Bertrand, P., Fontecilla-Camps, J., and Rousset, M. (2008) Experimental approaches to kinetics of gas diffusion in hydrogenase. Proc. Natl. Acad. Sci. USA 105: 11188-11193.
Matias, P.M., Soares, C.M., Saraiva, L.M., Coelho, R., Morais, J., Le Gall, J., and Carrondo, M.A. (2001) [NiFe] hydrogenase from Desulfovibrio desulfuricans ATCC 27774: gene sequencing, three-dimensional structure determination and refinement at 1.8 Å and modelling studies of its interaction with the tetrahaem cytochrome c₃. J. Biol. Inorg. Chem. 6: 63-81.
Ogata, H., Hirota, S., Nakahara, A., Komori, H., Shibata, N., Kato, T., Kano, K., and Higuchi, Y. (2005) Activation process of [NiFe] hydrogenase elucidated by high-resolution X-ray analyses: conversion of the ready to the unready state. Structure 13: 1635-1642.
Ogata, H., Mizoguchi, Y., Mizuno, N., Miki, K., Adachi, S.I., Yasuoka, N., Yagi, T., Yamauchi, O., Hirota, S., and Higuchi, Y. (2002) Structural studies of the carbon monoxide complex of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F: suggestion for the initial activation site for dihydrogen. J. Am. Chem. Soc. 124: 11628-11635.
Ogata, H., Nishikawa, K., and Lubitz, W. (2015) Hydrogens detected by subatomic resolution protein crystallography in a [NiFe] hydrogenase. Nature 520: 571-574.
Rousset, M., Montet, Y., Guigliarelli, B., Forget, N., Asso, M., Bertrand, P., Fontecilla-Camps, J.C., and Hatchikian, E.C. (1998) [3Fe-4S] to [4Fe-4S] cluster conversion in Desulfovibrio fructosovorans [NiFe] hydrogenase by site-directed mutagenesis. Proc. Natl. Acad. Sci. USA 95: 11625-11630.
Tatsuhiko, Y., Kimura, K., Daidoji, H., Sakai, F., Tamura, S., and Inokuchi, H. (1976) Properties of purified hydrogenase from the particulate fraction of Desulfovibrio vulgaris Miyazaki. J. Biochem. 79: 661-671.
Vincent, K.A., Parkin, A., Lenz, O., Albracht, S.P., Fontecilla-Camps, J.C., Cammack, R., Friedrich, B., and Armstrong, F.A. (2005) Electrochemical definitions of O₂ sensitivity and oxidative inactivation in hydrogenases. J. Am. Chem. Soc. 127: 18179-18189.
Volbeda, A., Martin, L., Cavazza, C., Matho, M., Faber, B.W., Roseboom, W., Albracht, S.P., Garcin, E., Rousset, M., and Fontecilla-Camps, J.C. (2005) Structural differences between the ready and unready oxidized states of [NiFe] hydrogenases. J. Biol. Inorg. Chem. 10: 239-249.
Volbeda, A., Montet, Y., Vernède, X., Hatchikian, E.C., and Fontecilla-Camps, J.C. (2002) High-resolution crystallographic analysis of Desulfovibrio fructosovorans [NiFe] hydrogenase. Int. J. Hydrogen Energy 27: 1449-1461.
Volbeda, A., Charon, M.H., Piras, C., Hatchikian, E.C., Frey, M., and Fontecilla-Camps, J.C. (1995) Crystal structure of the nickel-iron hydrogenase from Desulfovibrio gigas. Nature 373: 580-587.
Yagi, T., Honya, M. and Tamiya, N. (1968) Purification and properties of hydrogenases of different origins. BBA Bioenerget. 153: 699-705.
Yahata, N., Saitoh, T., Takayama, Y., Ozawa, K., Ogata, H., Higuchi, Y., and Akutsu, H. (2006) Redox interaction of cytochrome c₃ with [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. Biochem. 45: 1653-1662.

Chemistry:

Albracht, S.P.J., Kröger, A., Van der Zwaan, J.W., Unden, G., Böcher, R., Mell, H., and Fontijn, R.D. (1986) Direct evidence for sulphur as a ligand to nickel in hydrogenase: an EPR study of the enzyme from Wolinella succinogenes enriched in ³³S. BBA Prot. Struct. Mol. Enzymol. 874: 116-127.
Amara, P., Volbeda, A., Fontecilla-Camps, J.C., and Field, M.J. (1999) A hybrid density functional theory/molecular mechanics study of nickel-iron hydrogenase: investigation of the active site redox states. J. Am. Chem. Soc. USA 121: 4468-4477.
Bertrand, P., Dole, F., Asso, M., and Guigliarelli, B. (2000) Is there a rate-limiting step in the catalytic cycle of [Ni-Fe] hydrogenases? J. Biol. Inorg. Chem. 5: 682-691.
Cammack, R., Patil, D., Aguirre, R., and Hatchikian, E.C. (1982) Redox properties of the ESR-detectable nickel in hydrogenase from Desulfovibrio gigas. FEBS Lett. 142: 289-292.
Cammack, R., Patil, D.S., Hatchikian, E.C., and Fernández, V.M. (1987) Nickel and iron-sulphur centres in Desulfovibrio gigas hydrogenase: ESR spectra, redox properties and interactions. BBA Prot. Struct. Mol. Enzymol. 912: 98-109.
Carepo, M., Tierney, D.L., Brondino, C.D., Yang, T.C., Pamplona, A., Telser, J., Moura, I., Moura, J.J., and Hoffman, B.M. (2002) ¹⁷O ENDOR Detection of a solvent-derived Ni-(OH_x)-Fe bridge that is lost upon activation of the hydrogenase from Desulfovibrio gigas. J. Am. Chem. Soc. 124: 281-286.
de Lacey, A.L., Hatchikian, E.C., Volbeda, A., Frey, M., Fontecilla-Camps, J.C., and Fernandez, V.M. (1997) Infrared-spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio gigas. J. Am. Chem. Soc. 119: 7181-7189.
De Lacey, A.L., Fernandez, V.M., Rousset, M., Cavazza, C., and Hatchikian, C.E. (2003) Spectroscopic and kinetic characterization of active site mutants of Desulfovibrio fructosovorans Ni-Fe hydrogenase. J. Biol. Inorg. Chem. 8: 129-134.
De Lacey, A.L., Stadler, C., Fernandez, V.M., Hatchikian, C.E., Fan, H.J., Li, S., and Hall, M.B. (2002) IR spectroelectrochemical study of the binding of carbon monoxide to the active site of Desulfovibrio fructosovorans Ni-Fe hydrogenase. J. Biol. Inorg. Chem. 7: 318-326.
Fichtner, C., Laurich, C., Bothe, E., and Lubitz, W. (2006) Spectroelectrochemical characterization of the [NiFe] hydrogenase of Desulfovibrio vulgaris Miyazaki F. Biochem. 45: 9706-9716.
Fichtner, C., van Gastel, M., and Lubitz, W. (2003) Wavelength dependence of the photo-induced conversion of the Ni-C to the Ni-L redox state in the [NiFe] hydrogenase of Desulfovibrio vulgaris Miyazaki F. Phys. Chem. Chem. Phys. 5: 5507-5513.
Foerster, S., Stein, M., Brecht, M., Ogata, H., Higuchi, Y., and Lubitz, W. (2003) Single crystal EPR studies of the reduced active site of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J. Am. Chem. Soc. 125: 83-93.
Huynh, B.H., Patil, D.S., Moura, I., Teixeira, M., Moura, J.J., DerVartanian, D.V., Czechowski, M.H., Prickril, B.C., Peck, H.D., and LeGall, J. (1987) On the active sites of the [NiFe] hydrogenase from Desulfovibrio gigas. Mössbauer and redox-titration studies. J. Biol. Chem. 262: 795-800.
Léger, C., Dementin, S., Bertrand, P., Rousset, M., and Guigliarelli, B. (2004) Inhibition and aerobic inactivation kinetics of Desulfovibrio fructosovorans NiFe hydrogenase studied by protein film voltammetry. J. Am. Chem. Soc. 126: 12162-12172.
Li, S. and Hall, M.B. (2001) Predictions of the unready states of [NiFe] Desulfovibrio gigas hydrogenase from density functional theory. Inorg. Chem. 40: 18-24.
Millo, D., Pandelia, M.E., Utesch, T., Wisitruangsakul, N., Mroginski, M.A., Lubitz, W., Hildebrandt, P., and Zebger, I. (2009) Spectroelectrochemical study of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F in solution and immobilized on biocompatible gold surfaces. J. Phys. Chem. B 113: 15344-15351.
Niu, S. and Hall, M.B. (2001) The heterolytic bond cleavage of H₂ in the [NiFe] hydrogenase of Desulfovibrio gigas by a nucleophilic addition mechanism. Inorg. Chem. 40: 6201-6203.
Nishikawa, K., Mochida, S., Hiromoto, T., Shibata, N., and Higuchi, Y. (2017) Ni-elimination from the active site of the standard [NiFe]‑hydrogenase upon oxidation by O₂. J. Inorg. Biochem. 177: 435-437.
Ogata, H. et al (2015) Hydride bridge in [NiFe]-hydrogenase observed by nuclear resonance vibrational spectroscopy. Nat. Commun. 6: 7890.
Pandelia, M.E., Ogata, H., Currell, L.J., Flores, M., and Lubitz, W. (2010) Inhibition of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F by carbon monoxide: an FTIR and EPR spectroscopic study. BBA Bioenerg. 1797: 304-313.
Pandelia, M.E., Ogata, H., and Lubitz, W. (2010) Intermediates in the catalytic cycle of [NiFe] hydrogenase: functional spectroscopy of the active site. ChemPhysChem 11: 1127-1140.
Stein, M. and Lubitz, W. (2001) The electronic structure of the catalytic intermediate Ni-C in [NiFe] and [NiFeSe] hydrogenases. Phys. Chem. Chem. Phys. 3: 5115-5120.
Teixeira, M., Moura, I., Xavier, A.V., Moura, J.J., LeGall, J., DerVartanian, D.V., Peck, H.D., and Huynh, B.H. (1989) Redox intermediates of Desulfovibrio gigas [NiFe] hydrogenase generated under hydrogen. Mössbauer and EPR characterization of the metal centers. J. Biol. Chem. 264: 16435-16450.
Teixeira, M., Moura, I., Xavier, A.V., Huynh, B.H., DerVartanian, D.V., Peck, H.D., LeGall, J., and Moura, J.J. (1985) Electron paramagnetic resonance studies on the mechanism of activation and the catalytic cycle of the nickel-containing hydrogenase from Desulfovibrio gigas. J. Biol. Chem. 260: 8942-8950.
Trofanchuk, O., Stein, M., Gessner, C., Lendzian, F., Higuchi, Y., and Lubitz, W. (2000) Single crystal EPR studies of the oxidized active site of [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J. Biol. Inorg. Chem. 5: 36-44.
van Gastel, M., Stein, M., Brecht, M., Schröder, O., Lendzian, F., Bittl, R., Ogata, H., Higuchi, Y., and Lubitz, W. (2006) A single-crystal ENDOR and density functional theory study of the oxidized states of the [NiFe] hydrogenase from Desulfovibrio vulgaris Miyazaki F. J. Biol. Inorg. Chem. 11: 41-51.
Vincent, K.A., Belsey, N.A., Lubitz, W., and Armstrong, F.A. (2006) Rapid and reversible reactions of [NiFe]-hydrogenases with sulfide. J. Am. Chem. Soc. USA 128: 7448-7449.