[NiFe] Group 3a-hydrogenase

This entry was last updated at: Feb. 9, 2018, 7:13 a.m.

Properties

Group	[NiFe] Group 3: Cofactor-coupled bidirectional [NiFe] hydrogenases
Subgroup	[NiFe] Group 3a: F₄₂₀-coupled
Function	Directly couples oxidation of H₂ to reduction of F₄₂₀ during hydrogenotrophic methanogenesis. Reverse reaction proposed to occur during methylotrophic methanogenesis. Electrons flow between H₂-activating hydrogenase subunits to F₄₂₀ reductase subunit.
Activity	Bidirectional
Oxygen tolerance	O₂-tolerant
Localisation	Cytosolic

Distribution

Ecosystem distribution	Methanogenic environments such as anoxic soils, marine sediments, and gastrointestinal tracts
Taxonomic distribution	Encoded in all hydrogenotrophic methanogens

Genetic Organisation

e.g. Methanothermobacter marburgensis (WP_013296467.1):

Architecture

Structures	4OMF (Methanothermobacter marburgensis, 1.7 Å resolution, active) 4CI0 (Methanothermobacter marburgensis, 3.4 Å resolution, active) 3ZFS (Methanothermobacter marburgensis, 4.0 Å resolution, active)
Subunits	3
Subunit description	FrhA (hydrogenase large subunit) FrhG (hydrogenase small subunit) FrhB (F₄₂₀ reductase subunit)
Catalytic site	[NiFe]-centre or [NiFeSe]-centre
FeS clusters	Proximal: 4Cys[4Fe4S] or 3Cys1Asp[4Fe4S]

Important Notes

This subgroup also includes a small lineage of enzymes in Thermococci. As this order does not synthesize F₄₂₀, these hydrogenases presumably couple H₂ oxidation to the reduction of another flavin or nicotinamide compound.

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_015791787.1	Methanocaldococcus fervens	[NiFe] Group 3a	Euryarchaeota	Methanococcales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_016359193.1	Methanobrevibacter sp. AbM4	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_019262624.1	Methanobrevibacter smithii	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_012956862.1	Methanobrevibacter ruminantium	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_023993015.1	Methanobacterium sp. MB1	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_013826770.1	Methanobacterium paludis	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_013643821.1	Methanobacterium lacus	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_004029354.1	Methanobacterium formicicum	[NiFe] Group 3a	Euryarchaeota	Methanobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_013638061.1	Desulfurobacterium thermolithotrophum	[NiFe] Group 3a	Aquificae	Desulfurobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase
WP_022846160.1	Desulfurobacterium sp. TC5-1	[NiFe] Group 3a	Aquificae	Desulfurobacteriales	Anaerobic Uptake	Sensitive	3	[NiFe]-centre, 3 x [4Fe4S] clusters	F420 reductase

Literature

Genetics:

Berghöfer, Y., Agha-Amiri, K., and Klein, A. (1994) Selenium is involved in the negative regulation of the expression of selenium-free [NiFe] hydrogenases in Methanococcus voltae. Mol. Gen. Genet. 242: 369-373.
Halboth, S. and Klein, A. (1992) Methanococcus voltae harbors four gene clusters potentially encoding two [NiFe] and two [NiFeSe] hydrogenases, each of the cofactor F₄₂₀-reducing or F₄₂₀-non-reducing types. Mol. Gen. Genet. 233: 217-224.
Lee, S.H., Kim, M.S., Kim, Y.J., Kim, T.W., Kang, S.G., and Lee, H.S., 2017. Transcriptomic profiling and its implications for the H₂ production of a non-methanogen deficient in the frhAGB-encoding hydrogenase. Appl. Microbiol. Biotechnol. 101: 5081-5088.
Noll, I., Müller, S., and Klein, A. (1999) Transcriptional regulation of genes encoding the selenium-free [NiFe]-hydrogenases in the archaeon Methanococcus voltae involves positive and negative control elements. Genet. 152: 1335-1341.
Vignais, P.M., Billoud, B., and Meyer, J. (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25: 455-501.

Physiology:

Baron, S.F., Brown, D.P., and Ferry, J.G. (1987) Locations of the hydrogenases of Methanobacterium formicicum after subcellular fractionation of cell extract. J. Bacteriol. 169 3823-3825.
de Poorter, L.M.I., Geerts, W.J., and Keltjens, J.T. (2005) Hydrogen concentrations in methane-forming cells probed by the ratios of reduced and oxidized coenzyme F₄₂₀. Microbiol. 151: 1697-1705.
Hendrickson, E.L. and Leigh, J. (2008) Roles of coenzyme F₄₂₀-reducing hydrogenases and hydrogen- and F₄₂₀-dependent methylenetetrahydromethanopterin dehydrogenases in reduction of F₄₂₀ and production of hydrogen during methanogenesis. J. Bacteriol. 190: 4818-4821.
Kulkarni, G., Kridelbaugh, D.M., Guss, A.M., and Metcalf, W.W. (2009) Hydrogen is a preferred intermediate in the energy-conserving electron transport chain of Methanosarcina barkeri. Proc. Natl. Acad. Sci. USA 106: 15915-15920.
Jeon, J.H., et al. (2014) Characterization of the frhAGB-encoding hydrogenase from a non-methanogenic hyperthermophilic archaeon. Extremophiles 19: 109-118.
Lünsdorf, H., Niedrig, M., and Fiebig, K. (1991) Immunocytochemical localization of the coenzyme F₄₂₀-reducing hydrogenase in Methanosarcina barkeri Fusaro. J. Bacteriol. 173: 978-984.
Sorgenfrei, O., Müller, S., Pfeiffer, M., Sniezko, I., and Klein, A. (1997) The [NiFe] hydrogenases of Methanococcus voltae: Genes, enzymes and regulation. Arch. Microbiol. 167: 189-195.
Tzeng, S.F., Wolfe, R.S., and Bryant, M.P. (1975) Factor 420-dependent pyridine nucleotide-linked hydrogenase system of Methanobacterium ruminantium. J. Bacteriol. 121: 184-191.
Vaupel, M. and Thauer, R.K. (1998) Two F₄₂₀-reducing hydrogenases in Methanosarcina barkeri. Arch. Microbiol. 169: 201-205.

Biochemistry:

Allegretti, M., Mills, D.J., McMullan, G., Kühlbrandt, W., and Vonck, J. (2014) Atomic model of the F₄₂₀-reducing [NiFe] hydrogenase by electron cryo-microscopy using a direct electron detector. eLife 3: e01963.
Baron, S.F. and Ferry, J.G. (1989) Purification and properties of the membrane-associated coenzyme F₄₂₀-reducing hydrogenase from Methanobacterium formicicum. J. Bacteriol. 171: 3846-3853.
Braks, I.J., Hoppert, M., Roge, S., and Mayer, F. (1994) Structural aspects and immunolocalization of the F₄₂₀-reducing and non-F₄₂₀-reducing hydrogenases from Methanobacterium thermoautotrophicum Marburg. J. Bacteriol. 176: 7677-7687.
Fiebig, K. and Friedrich, B. (1989) Purification of the F₄₂₀-reducing hydrogenase from Methanosarcina barkeri (strain Fusaro). Eur. J. Biochem. 184: 79-88.
Greening, C., Ahmed, H.F., Mohamed, E.A., Lee, B.M., Pandey, G., Warden, A., Oakeshott, J.G., Taylor, M.C., and Jackson, C.J. (2016) Physiology, biochemistry, and applications of F₄₂₀ and F_o dependent redox reactions. Microbiol. Mol. Biol. Rev. 80: 451-493.
Jacobson, F.S., Daniels, L., Fox, J.A., Walsh, C.T., and Orme-Johnson, W.H. (1982) Purification and properties of an 8-hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum. J. Biol. Chem. 257: 3385-3388.
Mills, D.J., Vitt, S., Strauss, M., Shima, S., and Vonck, J. (2013) De novo modeling of the F₄₂₀-reducing [NiFe]-hydrogenase from a methanogenic archaeon by cryo-electron microscopy. eLife 2: e00218.
Muth, E., Mörschel, E., and Klein, A. (1987) Purification and characterization of an 8-hydroxy-5-deazaflavin-reducing hydrogenase from the archaebacterium Methanococcus voltae. Eur. J. Biochem. 169: 571-577.
Vitt, S., Ma, K., Warkentin, E., Moll, J., Pierik, A.J., Shima, S., and Ermler, U. (2014) The F₄₂₀-reducing [NiFe]-hydrogenase complex from Methanothermobacter marburgensis, the first X-ray structure of a group 3 family member. J. Mol. Biol. 426: 2813-26.
Walsh, C.T., Fox, J.A., Livingston, D.J., and Orme-Johnson, W.H. (1987) 8-Hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum: 1. Purification and characterization. Biochem. 26: 4219-4227.
Yamazaki, S. (1982) A selenium-containing hydrogenase from Methanococcus vannielii. Identification of the selenium moiety as a selenocysteine residue. J. Biol. Chem. 257: 7926-7929.
Yamazaki, S., Tsai, L., Stadtman, T.C., Teshima, T., Nakaji, A., and Shiba, T. (1985) Stereochemical studies of a selenium-containing hydrogenase from Methanococcus vannielii: determination of the absolute configuration of C-5 chirally labeled dihydro-8-hydroxy-5-deazaflavin cofactor. Proc. Natl. Acad. Sci. USA 82: 1364-1366.

Chemistry:

Kojima, N., Fox, J.A., Hausinger, R.P., Daniels, L., Orme-Johnson, W.H., and Walsh, C. (1983) Paramagnetic centers in the nickel-containing, deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum. Proc. Natl. Acad. Sci. USA 80: 378-382.
Lindahl, P.A., Kojima, N., Hausinger, R.P., Fox, J.A., Teo, B.K., Walsh, C.T., and Orme-Johnson, W.H. (1984) Nickel and iron EXAFS of F₄₂₀-reducing hydrogenase from Methanobacterium thermoautotrophicum. J. Am. Chem. Soc. 106: 3062-3064.
Livingston, D.J., Fox, J.A., Orme-Johnson, W.H., and Walsh, C.T. (1987) 8-hydroxy-5-deazaflavin-reducing hydrogenase from Methanobacterium thermoautotrophicum: 2. Kinetic and hydrogen-transfer studies. Derivation of a steady-state rate equation for deazaflavin-reducing hydrogenase. Biochem. 26: 4228-4237.
Sorgenfrei, O., Duin, E.C., Klein, A., and Albracht, S.P. (1997) Changes in the electronic structure around Ni in oxidized and reduced selenium-containing hydrogenases from Methanococcus voltae. Eur. J. Biochem. 247: 681-687.