[NiFe] Group 3d-hydrogenase

This entry was last updated at: Feb. 9, 2018, 6:37 a.m.

Properties

Group	[NiFe] Group 3: Cofactor-coupled bidirectional [NiFe] hydrogenases
Subgroup	[NiFe] Group 3d: NAD-coupled
Function	Generates reductant for hydrogenotrophic carbon-fixation by directly coupling oxidation of H₂ to reduction of NAD. Also acts in reverse direction to catalyse fermentative NADH-dependent production of H₂. Electrons flow between H₂-activating hydrogenase subunits to NAD-activating diaphorase subunits.
Activity	Bidirectional
Oxygen tolerance	O₂-tolerant
Localisation	Cytosolic

Distribution

Ecosystem distribution	Diverse soil and aquatic environments
Taxonomic distribution	Encoded in diverse Proteobacteria and Cyanobacteria

Genetic Organisation

e.g. Ralstonia eutropha (WP_011154013.1):

Architecture

Structures	5XF9 (Hydrogenophilus thermoluteolus, 2.6 Å resolution, oxidised) 5XFA (Hydrogenophilus thermoluteolus, 2.7 Å resolution, reduced)
Subunits	4 or 5
Subunit description	HoxH (hydrogenase large subunit) HoxY (hydrogenase small subunit) HoxF (diaphorase catalytic subunit) HoxU (diaphorase electron transfer subunit) Photosynthetic bacteria also contain HoxE (iron-sulfur subunit)
Catalytic site	[NiFe]-centre
FeS clusters	Proximal: 4Cys[4Fe4S] Medial: Absent Distal: Absent

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_006512117.1	Xenococcus sp. PCC 7305	[NiFe] Group 3d	Cyanobacteria	Pleurocapsales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_020393771.1	Thiothrix disciformis	[NiFe] Group 3d	Gammaproteobacteria	Thiotrichales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_009150973.1	Thiorhodovibrio sp. 970	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_007042613.1	Thiorhodococcus drewsii	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_023411848.1	Thiohalocapsa sp. PB-PSB1	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_015281226.1	Thioflavicoccus mobilis	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_014777645.1	Thiocystis violascens	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
ADK12981.1	Thiocapsa roseopersicina	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
AAP50523.1	Thiocapsa roseopersicina	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_007191642.1	Thiocapsa marina	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_007191859.1	Thiocapsa marina	[NiFe] Group 3d	Gammaproteobacteria	Chromatiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_014163745.1	Thermovirga lienii	[NiFe] Group 3d	Synergistetes	Synergistales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_012585448.1	Thauera sp. MZ1T	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_004252763.1	Thauera sp. 63	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_002929027.1	Thauera sp. 28	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_002937457.1	Thauera sp. 27	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_004363405.1	Thauera phenylacetica	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_004322153.1	Thauera aminoaromatica	[NiFe] Group 3d	Betaproteobacteria	Rhodocyclales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011699561.1	Syntrophobacter fumaroxidans	[NiFe] Group 3d	Deltaproteobacteria	Syntrophobacterales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_010872716.1	Synechocystis sp. PCC 6803	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_028947433.1	Synechocystis sp. PCC 6714	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_006170040.1	Synechococcus sp. WH 5701	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_017324543.1	Synechococcus sp. PCC 7336	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_012305837.1	Synechococcus sp. PCC 7002	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_024545803.1	Synechococcus sp. NKBG15041c	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_029552892.1	Synechococcus sp. CB0101	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011378516.1	Synechococcus elongatus	[NiFe] Group 3d	Cyanobacteria	Chroococcales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_022771893.1	Symbiobacter mobilis	[NiFe] Group 3d	Betaproteobacteria	Burkholderiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_021287226.1	Sulfurimonas sp. AST-10	[NiFe] Group 3d	Epsilonproteobacteria	Campylobacterales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_009205622.1	Sulfuricella denitrificans	[NiFe] Group 3d	Betaproteobacteria	Hydrogenophilales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_017305034.1	Spirulina subsalsa	[NiFe] Group 3d	Cyanobacteria	Oscillatoriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011686721.1	Solibacter usitatus	[NiFe] Group 3d	Acidobacteria	Solibacterales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_013029742.1	Sideroxydans lithotrophicus	[NiFe] Group 3d	Betaproteobacteria	Gallionellales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_023490135.1	Serratia sp. DD3	[NiFe] Group 3d	Gammaproteobacteria	Enterobacteriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_029133296.1	Sedimenticola selenatireducens	[NiFe] Group 3d	Gammaproteobacteria	Unclassified	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011958239.1	Roseiflexus sp. RS-1	[NiFe] Group 3d	Chloroflexi	Chloroflexales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_012119893.1	Roseiflexus castenholzii	[NiFe] Group 3d	Chloroflexi	Chloroflexales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_008384205.1	Rhodovulum sp. PH10	[NiFe] Group 3d	Alphaproteobacteria	Rhodobacterales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011466117.1	Rhodoferax ferrireducens	[NiFe] Group 3d	Betaproteobacteria	Burkholderiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_009341606.1	Raphidiopsis brookii	[NiFe] Group 3d	Cyanobacteria	Nostocales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011154013.1	Ralstonia eutropha	[NiFe] Group 3d	Betaproteobacteria	Burkholderiales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_011769610.1	Psychromonas ingrahamii	[NiFe] Group 3d	Gammaproteobacteria	Alteromonadales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_028864775.1	Psychromonas aquimarina	[NiFe] Group 3d	Gammaproteobacteria	Alteromonadales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_019498425.1	Pseudanabaena sp. PCC 6802	[NiFe] Group 3d	Cyanobacteria	Oscillatoriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_019509061.1	Pleurocapsa sp. PCC 7319	[NiFe] Group 3d	Cyanobacteria	Pleurocapsales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_015144267.1	Pleurocapsa minor	[NiFe] Group 3d	Cyanobacteria	Pleurocapsales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_006562473.1	Oscillochloris trichoides	[NiFe] Group 3d	Chloroflexi	Chloroflexales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_017715405.1	Oscillatoria sp. PCC 10802	[NiFe] Group 3d	Cyanobacteria	Oscillatoriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_015175286.1	Oscillatoria nigro-viridis	[NiFe] Group 3d	Cyanobacteria	Oscillatoriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein
WP_015151979.1	Oscillatoria acuminata	[NiFe] Group 3d	Cyanobacteria	Oscillatoriales	Bidirectional	Tolerant	4	[NiFe]-centre, 1 x [4Fe4S] clusters	Diaphorase, [FeS] protein

Literature

Genetics:

Boison, G., Bothe, H., and 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.
Boison, G., Schmitz, O., Mikheeva, L., Shestakov, S., and Bothe, H. (1996) Cloning, molecular analysis and insertional mutagenesis of the bidirectional hydrogenase genes from the cyanobacterium Anacystis nidulans. FEBS Lett. 394: 153-158.
Boison, G., Schmitz, O., Schmitz, B., and Bothe, H. (1998) Unusual gene arrangement of the bidirectional hydrogenase and functional analysis of its diaphorase subunit HoxU in respiration of the unicellular cyanobacterium Anacystis nidulans. Curr. Microbiol. 36: 253-258.
Eberz, G., Hogrefe, C., Kortlüke, C., Kamienski, A., and Friedrich, B. (1986) Molecular cloning of structural and regulatory hydrogenase (hox) genes of Alcaligenes eutrophus H16. J. Bacteriol. 168: 636-641.
Eckert, C., Boehm, M., Carrieri, D., Yu, J., Dubini, A., Nixon, P.J., and Maness, P.C. (2012) Genetic analysis of the Hox hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 reveals subunit roles in association, assembly, maturation, and function. J. Biol. Chem. 287: 43502-43515.
Gutekunst, K., Phunpruch, S., Schwarz, C., Schuchardt, S., Schulz-Friedrich, R., and Appel, J. (2005) LexA regulates the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803 as a transcription activator. Mol. Microbiol. 58: 810-823.
Grzeszik, C., Lübbers, M., Reh, M. and Schlegel, H.G. (1997) Genes encoding the NAD-reducing hydrogenase of Rhodococcus opacus MR11. Microbiol. 143: 1271-1286.
Hogrefe, C., Römermann, D., and Friedrich, B. (1984) Alcaligenes eutrophus hydrogenase genes (Hox). J. Bacteriol. 158: 43-48.
Maróti, J., Farkas, A., Nagy, I.K., Maróti, G., Kondorosi, É., Rákhely, G., and Kovács, K.L. (2010) A second soluble Hox-type NiFe enzyme completes the hydrogenase set in Thiocapsa roseopersicina BBS. Appl. Environ. Microbiol. 76: 5113-5123.
Oliveira, P. and Lindblad, P. (2005) LexA, a transcription regulator binding in the promoter region of the bidirectional hydrogenase in the cyanobacterium Synechocystis sp. PCC 6803. FEMS Microbiol. Lett. 251: 59-66.
Oliveira, P. and Lindblad, P. (2009) Transcriptional regulation of the cyanobacterial bidirectional Hox-hydrogenase. Dalton Trans. 45: 9990-9996.
Schmitz, O., Boison, G., and 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.
Schmitz, O., Boison, G., Hilscher, R., Hundeshagen, B., Zimmer, W., Lottspeich, F., and Bothe, H. (1995) Molecular biological analysis of a bidirectional hydrogenase from cyanobacteria. Eur. J. Biochem. 233: 266-276.
Sheremetieva, M.E., Troshina, O.Y., Serebryakova, L.T., and Lindblad, P. (2002) Identification of hox genes and analysis of their transcription in the unicellular cyanobacterium Gloeocapsa alpicola CALU 743 growing under nitrate-limiting conditions. FEMS Microbiol. Lett. 214: 229-233
Sjöholm, J., Oliveira, P., and Lindblad, P. (2007) Transcription and regulation of the bidirectional hydrogenase in the cyanobacterium Nostoc sp. strain PCC 7120. Appl. Environ. Microbiol. 73: 5435-5446
Tran-Betcke, A., Warnecke, U., Böcker, C., Zaborosch, C., and Friedrich, B. (1990) Cloning and nucleotide sequences of the genes for the subunits of NAD-reducing hydrogenase of Alcaligenes eutrophus H16. J. Bacteriol. 172: 2920-2929.
Vignais, P.M., Billoud, B., and Meyer, J. (2001) Classification and phylogeny of hydrogenases. FEMS Microbiol. Rev. 25: 455-501.
Wells, M.A., Mercer, J., Mott, R.A., Pereira-Medrano, A.G., Burja, A.M., Radianingtyas, H., and Wright, P.C. (2011) Engineering a non-native hydrogen production pathway into Escherichia coli via a cyanobacterial [NiFe] hydrogenase. Metab. Eng. 13: 445-453.

Physiology:

Aggag, M. and Schlegel, H.G. (1973) Studies on a gram-positive hydrogen bacterium, Nocardia opaca strain 1b. Arch. Microbiol. 88: 299-318.
Antal, T.K. and Lindblad, P. (2005) Production of H₂ by sulphur-deprived cells of the unicellular cyanobacteria Gloeocapsa alpicola and Synechocystis sp. PCC 6803 during dark incubation with methane or at various extracellular pH. J. Appl. Microbiol. 98: 114-120.
Aubert-Jousset, E., Cano, M., Guedeney, G., Richaud, P., and Cournac, L. (2011) Role of HoxE subunit in Synechocystis PCC6803 hydrogenase. FEBS J. 278: 4035-4043.
Boison, G., Bothe, H., Hansel, A., and Lindblad, P. (1999) Evidence against a common use of the diaphorase subunits by the bidirectional hydrogenase and by the respiratory complex I in cyanobacteria. FEMS Microbiol. Lett. 174: 159-165.
Carrieri, D., Wawrousek, K., Eckert, C., Yu, J., and Maness, P.C. (2011) The role of the bidirectional hydrogenase in cyanobacteria. Bioresource Technol. 102: 8368-8377.
De Rosa, E., Checchetto, V., Franchin, C., Bergantino, E., Berto, P., Szabò, I., Giacometti, G.M., Arrigoni, G., and Costantini, P. (2015) [NiFe]-hydrogenase is essential for cyanobacterium Synechocystis sp. PCC 6803 aerobic growth in the dark. Sci. Rep. 5: 12424.
Friedrich, C.G., Friedrich, B. and Bowien, B. (1981) Formation of enzymes of autotrophic metabolism during heterotrophic growth of Alcaligenes eutrophus. Microbiol. 122: 69-78.
Grzeszik, C., Ross, K., Schneider, K., Reh, M., and Schlegel, H.G. (1997) Location, catalytic activity, and subunit composition of NAD-reducing hydrogenases of some Alcaligenes strains and Rhodococcus opacus MR22. Arch. Microbiol. 167: 172-176.
Gutekunst, K., Chen, X., Schreiber, K., Kaspar, U., Makam, S., and Appel, J. (2014) The bidirectional NiFe-hydrogenase in Synechocystis sp. PCC 6803 is reduced by flavodoxin and ferredoxin and is essential under mixotrophic, nitrate-limiting conditions. J. Biol. Chem. 289: 1930-1937.
Hanczár, T., Csáki, R., Bodrossy, L., Murrell, C.J., and Kovács, K.L. (2002) Detection and localization of two hydrogenases in Methylococcus capsulatus (Bath) and their potential role in methane metabolism. Arch. Microbiol. 177: 167-172.
Houchins, J.P. and Burris, R.H. (1981) Occurrence and localization of two distinct hydrogenases in the heterocystous cyanobacterium Anabaena sp. strain 7120. J. Bacteriol. 146: 209-214.
Laurinavichene, T.V., Rákhley, G., Kovács, K.L., and Tsygankov, A.A. (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: 403-410.
Mori, J.F., Scott, J.J., Hager, K.W., Moyer, C.L., Küsel, K., and Emerson, D. (2017) Physiological and ecological implications of an iron-or hydrogen-oxidizing member of the Zetaproteobacteria, Ghiorsea bivora, gen. nov., sp. nov. ISME J. 11: 2624-2636.
Pálágyi-Mészáros, L.S., Maróti, J., Latinovics, D., Balogh, T., Klement, E., Medzihradszky, K.F., Rákhely, G., and Kovács, K.L. (2009) Electron-transfer subunits of the NiFe hydrogenases in Thiocapsa roseopersicina BBS. FEBS J. 276: 164-174.
Papen, H., Kentemich, T., Schmülling, T. and Bothe, H. (1986) Hydrogenase activities in cyanobacteria. Biochimie 68: 121-132.
Porthun, A., Bernhard, M., and Friedrich, B. (2002) Expression of a functional NAD-reducing [NiFe] hydrogenase from the gram-positive Rhodococcus opacus in the gram-negative Ralstonia eutropha. Arch. Microbiol. 177: 159-166.
Rákhely, G., Kovács, A.T., Maroti, G., Fodor, B.D., Csanádi, G., Latinovics, D., and Kovács, K.L. (2004) Cyanobacterial-type, heteropentameric, NAD⁺-reducing NiFe hydrogenase in the purple sulfur photosynthetic bacterium Thiocapsa roseopersicina. Appl. Environ. Microbiol. 70: 722-728.
Rákhely, G., Laurinavichene, T.V., Tsygankov, A.A., and Kovács, K.L. (2007) The role of Hox hydrogenase in the H₂ metabolism of Thiocapsa roseopersicina. BBA Bioenerg. 1767: 671-676.
Schmitz, O. and Bothe, H. (1996) NAD(P)⁺-dependent hydrogenase activity in extracts from the cyanobacterium Anacystis nidulans. FEMS Microbiol. Lett. 135: 97-101.
Schütz, K., Happe, T., Troshina, O., Lindblad, P., Leitão, E., Oliveira, P., and Tamagnini, P. (2004) Cyanobacterial H₂ production—a comparative analysis. Planta 218: 350-359.
Tamagnini, P., Leitão, E., Oliveira, P., Ferreira, D., Pinto, F., Harris, D.J., Heidorn, T., and Lindblad, P. (2007) Cyanobacterial hydrogenases: diversity, regulation and applications. FEMS Microbiol. Rev. 31: 692-720.

Biochemistry:

Burgdorf, T., van der Linden, E., Bernhard, M., Yin, Q.Y., Back, J.W., Hartog, A.F., Muijsers, A.O., de Koster, C.G., Albracht, S.P., and Friedrich, B. (2005) The soluble NAD⁺-reducing [NiFe]-hydrogenase from Ralstonia eutropha H16 consists of six subunits and can be specifically activated by NADPH. J. Bacteriol. 187: 3122-3132.
Germer, F., Zebger, I., Saggu, M., Lendzian, F., Schulz, R., and Appel, J. (2009) Overexpression, isolation, and spectroscopic characterization of the bidirectional [NiFe] hydrogenase from Synechocystis sp. PCC 6803. J. Biol. Chem. 284: 36462-36472.
Karstens, K., Wahlefeld, S., Horch, M., Grunzel, M., Lauterbach, L., Lendzian, F., Zebger, I., and Lenz, O. (2015) Impact of the iron-sulfur cluster proximal to the active site on the catalytic function of an O₂-tolerant NAD⁺-reducing [NiFe]-hydrogenase. Biochem. 54: 389-403.
Horch, M., Lauterbach, L., Lenz, O., Hildebrandt, P., and Zebger, I. (2012) NAD(H)-coupled hydrogen cycling: structure-function relationships of bidirectional [NiFe] hydrogenases. FEBS Lett. 586: 545-556.
Horch, M., Lauterbach, L., Mroginski, M.A., Hildebrandt, P., Lenz, O., and Zebger, I. (2015) Reversible active site sulfoxygenation can explain the oxygen tolerance of a NAD⁺-reducing [NiFe] hydrogenase and its unusual infrared spectroscopic properties. J. Am. Chem. Soc. 137: 2555-2564.
Lauterbach, L. and Lenz, O. (2013) Catalytic production of hydrogen peroxide and water by oxygen-tolerant [NiFe]-hydrogenase during H₂ cycling in the presence of O₂. J. Am. Chem. Soc. 135: 17897-17905.
Lauterbach, L., Idris, Z., Vincent, K.A., and Lenz, O. (2011) Catalytic properties of the isolated diaphorase fragment of the NAD⁺-reducing [NiFe]-hydrogenase from Ralstonia eutropha. PLOS One 6: e25939.
Lauterbach, L., Lenz, O. and Vincent, K.A. (2013) H₂-driven cofactor regeneration with NAD(P)⁺-reducing hydrogenases. FEBS J. 280: 3058-3068.
Lauterbach, L., Liu, J., Horch, M., Hummel, P., Schwarze, A., Haumann, M., Vincent, K.A., Lenz, O., and Zebger, I. (2011) The hydrogenase subcomplex of the NAD⁺-reducing [NiFe] hydrogenase from Ralstonia eutropha—insights into catalysis and redox interconversions. Eur. J. Inorg. Chem. 7: 1067-1079.
Löscher, S., Burgdorf, T., Zebger, I., Hildebrandt, P., Dau, H., Friedrich, B., and Haumann, M. (2006) Bias from H₂ cleavage to production and coordination changes at the Ni-Fe active site in the NAD⁺-reducing hydrogenase from Ralstonia eutropha. Biochem. 45: 11658-11665.
Massanz, C. and Friedrich, B. (1999) Amino acid replacements at the H₂-activating site of the NAD-reducing hydrogenase from Alcaligenes eutrophus. Biochem. 38: 14330-14337.
McIntosh, C.L., Germer, F., Schulz, R., Appel, J., and Jones, A.K. (2011) The [NiFe]-hydrogenase of the cyanobacterium Synechocystis sp. PCC 6803 works bidirectionally with a bias to H₂ production. J. Am. Chem. Soc. 133: 11308-11319.
Preissler, J., Wahlefeld, S., Lorent, C., Teutloff, C., Horch, M., Lauterbach, L., Cramer, S.P., Zebger, I., and Lenz, O. (2018) Enzymatic and spectroscopic properties of a thermostable [NiFe]‑hydrogenase performing H₂-driven NAD⁺-reduction in the presence of O2. BBA Bioenerg. 1859: 8-18.

Ratzka, J., Lauterbach, L., Lenz, O., and Ansorge-Schumacher, M.B. (2011) Systematic evaluation of the dihydrogen-oxidising and NAD⁺-reducing soluble [NiFe]-hydrogenase from Ralstonia eutropha H16 as a cofactor regeneration catalyst. Biocat. Biotransf. 29: 246-252.

Schmitz, O., Boison, G., Salzmann, H., Bothe, H., Schütz, K., Wang, S.H., and Happe, T (2002) HoxE - a subunit specific for the pentameric bidirectional hydrogenase complex (HoxEFUYH) of cyanobacteria. BBA Bioenerg. 1554: 66-74.

Schneider, K. and Schlegel, H.G. (1976) Purification and properties of soluble hydrogenase from Alcaligenes eutrophus H16. BBA Enzymol. 452: 66-80.

Schneider, K., Cammack, R., and Schlegel, H.G. (1984) Content and localization of FMN, Fe-S clusters and nickel in the NAD-linked hydrogenase of Nocardia opaca 1b. Eur. J. Biochem. 142: 75-84.

Schneider, K., Cammack, R., Schlegel, H.G., and Hall, D.O. (1979) The iron-sulphur centres of soluble hydrogenase from Alcaligenes eutrophus. BBA Prot. Struct. 578: 445-461.

Shomura, Y., Taketa, M., Nakashima, H., Tai, H., Nakagawa, H., Ikeda, Y., Ishii, M., Igarashi, Y., Nishihara, H., Yoon, K.S., Ogo, S., Hirota, S., and Higuchi, Y. (2017) Structural basis of the redox switches in the NAD⁺-reducing soluble [NiFe]-hydrogenase. Science 357: 928-932

Chemistry:

Erkens, A., Schneider, K., and Müller, A. (1996) The NAD-linked soluble hydrogenase from Alcaligenes eutrophus H16: detection and characterization of EPR signals deriving from nickel and flavin. J. Biol. Inorg. Chem. 1: 99-110.

Long, M., Liu, J., Chen, Z., Bleijlevens, B., Roseboom, W. and Albracht, S.P. (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.

Horch, M., Lauterbach, L., Saggu, M., Hildebrandt, P., Lendzian, F., Bittl, R., Lenz, O., and Zebger, I., 2010. Probing the active site of an O₂-tolerant NAD⁺-reducing [NiFe]-hydrogenase from Ralstonia eutropha H16 by in situ EPR and FTIR spectroscopy. Angewandte Chemie 49: 8026-8029.

Horch, M., Rippers, Y., Mroginski, M.A., Hildebrandt, P., and Zebger, I. (2013) Combining spectroscopy and theory to evaluate structural models of metalloenzymes: a case study on the soluble [NiFe] hydrogenase from Ralstonia eutropha. ChemPhysChem 14: 185-191.

Lauterbach, L., Wang, H., Horch, M., Gee, L.B., Yoda, Y., Tanaka, Y., Zebger, I., Lenz, O., and Cramer, S.P. (2015) Nuclear resonance vibrational spectroscopy reveals the FeS cluster composition and active site vibrational properties of an O₂-tolerant NAD⁺-reducing [NiFe] hydrogenase. Chem. Sci. 6: 1055-1060.

Löwenstein, J., Lauterbach, L., Teutloff, C., Lenz, O., and Bittl, R. (2015). Active site of the NAD⁺-reducing hydrogenase from Ralstonia eutropha studied by EPR spectroscopy. J. Phys. Chem. B 119: 13834-13841.

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