Home Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster
Article
Licensed
Unlicensed Requires Authentication

Heterodisulfide reductase from methanogenic archaea: a new catalytic role for an iron-sulfur cluster

  • Reiner Hedderich , Nils Hamann and Marina Bennati
Published/Copyright: October 12, 2005
Biological Chemistry
From the journal Volume 386 Issue 10

Abstract

Heterodisulfide reductase (HDR) from methanogenic archaea is an iron-sulfur protein that catalyzes reversible reduction of the heterodisulfide (CoM-S-S-CoB) of the methanogenic thiol-coenzymes, coenzyme M (CoM-SH) and coenzyme B (CoB-SH). Via the characterization of a paramagnetic reaction intermediate generated upon oxidation of the enzyme in the presence of coenzyme M, the enzyme was shown to contain a [4Fe-4S] cluster in its active site that catalyzes reduction of the disulfide substrate in two one-electron reduction steps. The formal thiyl radical generated by the initial one-electron reduction of the disulfide is stabilized via reduction and coordination of the resultant thiol to the [4Fe-4S] cluster.

:

Corresponding author

References

Bäumer, S., Murakami, E., Brodersen, J., Gottschalk, G., Ragsdale, S.W., and Deppenmeier, U. (1998). The F420H2:heterodisulfide oxidoreductase system from Methanosarcina species. 2-Hydroxyphenazine mediates electron transfer from F420H2 dehydrogenase to heterodisulfide reductase. FEBS Lett.428, 295–298.Search in Google Scholar

Beinert, H. (2000). Iron-sulfur proteins: ancient structures, still full of surprises. J. Biol. Inorg. Chem.5, 2–15.10.1007/s007750050002Search in Google Scholar

Bennati, M., Weiden, N., Dinse, K.P., and Hedderich, R. (2004). 57Fe ENDOR spectroscopy on the iron-sulfur cluster involved in substrate reduction of heterodisulfide reductase. J. Am. Chem. Soc.126, 8378–8379.10.1021/ja0498179Search in Google Scholar

Boll, M., Fuchs, G., and Lowe, D.J. (2001). Single turnover EPR studies of benzoyl-CoA reductase. Biochemistry40, 7612–7620.10.1021/bi002771lSearch in Google Scholar

Cole, S.T., Eiglmeier, K., Ahmed, S., Honore, N., Elmes, L., Anderson, W.F., and Weiner, J.H. (1988). Nucleotide sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K-12. J. Bacteriol.170, 2448–2456.10.1128/jb.170.6.2448-2456.1988Search in Google Scholar

Cosper, N.J., Booker, S.J., Ruzicka, F., Frey, P.A., and Scott, R.A. (2000). Direct FeS cluster involvement in generation of a radical in lysine 2,3-aminomutase. Biochemistry39, 15668–15673.10.1021/bi0022184Search in Google Scholar

Dai, S., Schwendtmayer, C., Schurmann, P., Ramaswamy, S., and Eklund, H. (2000). Redox signaling in chloroplasts: cleavage of disulfides by an iron-sulfur cluster. Science287, 655–658.10.1126/science.287.5453.655Search in Google Scholar

Deckert, G., Warren, P.V., Gaasterland, T., Young, W.G., Lenox, A.L., Graham, D.E., Overbeek, R., Snead, M.A., Keller, M., Aujay, M., et al. (1998). The complete genome of the hyperthermophilic bacterium Aquifex aeolicus. Nature392, 353–358.10.1038/32831Search in Google Scholar

Deppenmeier, U., Lienard, T., and Gottschalk, G. (1999). Novel reactions involved in energy conservation by methanogenic archaea. FEBS Lett.457, 291–297.10.1016/S0014-5793(99)01026-1Search in Google Scholar

Droux, M., Jacquot, J.P., Miginac-Maslow, M., Gadal, P., Huet, J.C., Crawford, N.A., Yee, B.C., and Buchanan, B.B. (1987). Ferredoxin-thioredoxin reductase, an iron-sulfur enzyme linking light to enzyme regulation in oxygenic photosynthesis: purification and properties of the enzyme from C3, C4, and cyanobacterial species. Arch. Biochem. Biophys.252, 426–439.10.1016/0003-9861(87)90049-XSearch in Google Scholar

Duin, E.C., Madadi-Kahkesh, S., Hedderich, R., Clay, M.D., and Johnson, M.K. (2002). Heterodisulfide reductase from Methanothermobacter marburgensis contains an active-site [4Fe-4S] cluster that is directly involved in mediating hetero-disulfide reduction. FEBS Lett.512, 263–268.10.1016/S0014-5793(02)02281-0Search in Google Scholar

Duin, E.C., Bauer, C., Jaun, B., and Hedderich, R. (2003). Coenzyme M binds to a [4Fe-4S] cluster in the active site of heterodisulfide reductase as deduced from EPR studies with the [33S]coenzyme M-treated enzyme. FEBS Lett.538, 81–84.10.1016/S0014-5793(03)00134-0Search in Google Scholar

Fontecave, M., Mulliez, E., and Ollagnier-de-Choudens, S. (2001). Adenosylmethionine as a source of 5′-deoxyadenosyl radicals. Curr. Opin. Chem. Biol.5, 506–511.10.1016/S1367-5931(00)00237-4Search in Google Scholar

Hedderich, R., Berkessel, A., and Thauer, R.K. (1990). Purification and properties of heterodisulfide reductase from Methanobacterium thermoautotrophicum (strain Marburg). Eur. J. Biochem.193, 255–261.10.1111/j.1432-1033.1990.tb19331.xSearch in Google Scholar PubMed

Hedderich, R., Koch, J., Linder, D., and Thauer, R.K. (1994). The heterodisulfide reductase from Methanobacterium thermo-autotrophicum contains sequence motifs characteristic of pyridine nucleotide-dependent thioredoxin reductases. Eur. J. Biochem.225, 253–261.10.1111/j.1432-1033.1994.00253.xSearch in Google Scholar PubMed

Hedderich, R., Klimmek, O., Kröger, A., Dirmeier, R., Keller, M., and Stetter, K.O. (1998). Anaerobic respiration with elemental sulfur and with disulfides. FEMS Microbiol. Rev.22, 353–381.10.1111/j.1574-6976.1998.tb00376.xSearch in Google Scholar

Heiden, S., Hedderich, R., Setzke, E., and Thauer, R.K. (1994). Purification of a two-subunit cytochrome-b-containing heterodisulfide reductase from methanol-grown Methanosarcina barkeri. Eur. J. Biochem.221, 855–861.10.1111/j.1432-1033.1994.tb18800.xSearch in Google Scholar PubMed

Heim, S., Künkel, A., Thauer, R.K., and Hedderich, R. (1998). Thiol:fumarate reductase (Tfr) from Methanobacterium thermoautotrophicum. Identification of the catalytic sites for fumarate reduction and thiol oxidation. Eur. J. Biochem.253, 292–299.Search in Google Scholar

Ide, T., Bäumer, S., and Deppenmeier, U. (1999). Energy conservation by the H2:heterodisulfide oxidoreductase from Methanosarcina mazei Gö1: identification of two proton-translocating segments. J. Bacteriol.181, 4076–4080.10.1128/JB.181.13.4076-4080.1999Search in Google Scholar PubMed PubMed Central

Iwasaki, T., Kounosu, A., Aoshima, M., Ohmori, D., Imai, T., Urushiyama, A., Cosper, N.J., and Scott, R.A. (2002). Novel [2Fe-2S]-type redox center C in SdhC of archaeal respiratory complex II from Sulfolobus tokodaii strain 7. J. Biol. Chem.277, 39642–39648.10.1074/jbc.M207312200Search in Google Scholar PubMed

Jameson, G.N., Walters, E.M., Manieri, W., Schurmann, P., Johnson, M.K., and Huynh, B.H. (2003). Spectroscopic evidence for site specific chemistry at a unique iron site of the [4Fe-4S] cluster in ferredoxin:thioredoxin reductase. J. Am. Chem. Soc.125, 1146–1147.10.1021/ja029338eSearch in Google Scholar PubMed

Janssen, S., Schafer, G., Anemüller, S., and Moll, R. (1997). A succinate dehydrogenase with novel structure and properties from the hyperthermophilic archaeon Sulfolobus acidocaldarius: genetic and biophysical characterization. J. Bacteriol.179, 5560–5569.10.1128/jb.179.17.5560-5569.1997Search in Google Scholar PubMed PubMed Central

Johnson, M.K., Duderstadt, R.E., and Duin, E.C. (1999). Biological and synthetic [Fe3S4] clusters. In: Advances in Inorganic Chemistry, A.G. Sykes and R. Cammack, eds. (New York, USA: Academic Press), pp. 1–73.10.1016/S0898-8838(08)60076-8Search in Google Scholar

Kappl, R., Ciurli, S., Luchinat, C., and Hüttermann, J. (1999). Probing structural and electronic properties of the oxidized [4Fe-4S]3+ cluster of Ectothiorhodospira halophila iso-II high-potential iron-sulfur protein by ENDOR spectroscopy. J. Am. Chem. Soc.121, 1925–1935.10.1021/ja980442zSearch in Google Scholar

Klenk, H.-P., Clayton, R.A., Tomb, J.F., White, O., Nelson K.E., Ketchum, K.A., Dodson, R.J., Gwinn, M., Hickey, E.K., Peterson, J.D., et al. (1997). The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus. Nature390, 364–370.10.1038/37052Search in Google Scholar PubMed

Künkel, A., Vaupel, M., Heim, S., Thauer, R.K., and Hedderich, R. (1997). Heterodisulfide reductase from methanol-grown cells of Methanosarcina barkeri is not a flavoenzyme. Eur. J. Biochem.244, 226–234.10.1111/j.1432-1033.1997.00226.xSearch in Google Scholar PubMed

Kunst, F., Ogasawara, N., Moszer, I., Albertini, A.M., Alloni, G., Azevedo, V., Bertero, M.G., Bessieres, P., Bolotin, A., Borchert, S., et al. (1997). The complete genome sequence of the Gram-positive bacterium Bacillus subtilis. Nature390, 249–256.10.1038/36786Search in Google Scholar PubMed

Lemos, R.S., Gomes, C.M., and Teixeira, M. (2001). Acidianus ambivalens complex II typifies a novel family of succinate dehydrogenases. Biochem. Biophys. Res. Commun.281, 141–150.10.1006/bbrc.2001.4317Search in Google Scholar PubMed

Madadi-Kahkesh, S., Duin, E.C., Heim, S., Albracht, S.P.J., Johnson, M.K., and Hedderich, R. (2001). A paramagnetic species with unique EPR characteristics in the active site of heterodisulfide reductase from methanogenic archaea. Eur. J. Biochem.268, 2566–2577.10.1046/j.1432-1327.2001.02141.xSearch in Google Scholar PubMed

Mander, G.J., Duin, E.C., Linder, D., Stetter, K.O., and Hedderich, R. (2002). Purification and characterization of a membrane-bound enzyme complex from the sulfate-reducing archaeon Archaeoglobus fulgidus related to heterodisulfide reductase from methanogenic archaea. Eur. J. Biochem.269, 1895–1904.10.1046/j.1432-1033.2002.02839.xSearch in Google Scholar PubMed

Mander, G.J., Pierik, A.J., Huber, H., and Hedderich, R. (2004). Two distinct heterodisulfide reductase-like enzymes in the sulfate-reducing archaeon Archaeoglobus profundus. Eur. J. Biochem.271, 1106–1116.10.1111/j.1432-1033.2004.04013.xSearch in Google Scholar PubMed

Nakamura, Y., Kaneko, T., Hirosawa, M., Miyajima, N., and Tabata, S. (1998). CyanoBase, a www database containing the complete nucleotide sequence of the genome of Synechocystis sp. strain PCC6803. Nucleic Acids Res.26, 63–67.10.1093/nar/26.1.63Search in Google Scholar PubMed PubMed Central

Pellicer, M.T., Badia, J., Aguilar, J., and Baldoma, L. (1996). glc locus of Escherichia coli: characterization of genes encoding the subunits of glycolate oxidase and the glc regulator protein. J. Bacteriol.178, 2051–2059.10.1128/jb.178.7.2051-2059.1996Search in Google Scholar PubMed PubMed Central

Pott, A.S. and Dahl, C. (1998). Sirohaem sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology144, 1881–1894.10.1099/00221287-144-7-1881Search in Google Scholar PubMed

Rakhely, G., Colbeau, A., Garin, J., Vignais, P.M., and Kovacs, K.L. (1998). Unusual organization of the genes coding for HydSL, the stable [NiFe]hydrogenase in the photosynthetic bacterium Thiocapsa roseopersicina BBS. J. Bacteriol.180, 1460–1465.10.1128/JB.180.6.1460-1465.1998Search in Google Scholar PubMed PubMed Central

Rius, G. and Lamotte, B. (1989). Single-crystal ENDOR study of a 57Fe-enriched iron-sulfur [4Fe-4S]3+ cluster. J. Am. Chem. Soc.111, 2464–2469.10.1021/ja00189a015Search in Google Scholar

Rossi, M., Pollock, W.B., Reij, M.W., Keon, R.G., Fu, R., and Voordouw, G. (1993). The hmc operon of Desulfovibrio vulgaris subsp. vulgaris Hildenborough encodes a potential transmembrane redox protein complex. J. Bacteriol.175, 4699–4711.Search in Google Scholar

Schürmann, P., Stritt-Etter, A.L., and Li, J. (1995). Reduction of ferredoxin:thioredoxin reductase by artificial electron donors. Photosynth. Res.309, 309–312.10.1007/BF00020445Search in Google Scholar PubMed

Setzke, E., Hedderich, R., Heiden, S., and Thauer, R.K. (1994). H2:heterodisulfide oxidoreductase complex from Methanobacterium thermoautotrophicum: composition and properties. Eur. J. Biochem.220, 139–148.10.1111/j.1432-1033.1994.tb18608.xSearch in Google Scholar PubMed

Shokes, J.E., Duin, E.C., Bauer, C., Jaun, B., Hedderich, R., Koch, J., and Scott, R.A. (2005). Direct interaction of coenzyme M with the active-site Fe-S cluster of heterodisulfide reductase. FEBS Lett.579, 1741–1744.10.1016/j.febslet.2005.02.034Search in Google Scholar PubMed

Simianu, M., Murakami, E., Brewer, J.M., and Ragsdale, S.W. (1998). Purification and properties of the heme- and iron-sulfur-containing heterodisulfide reductase from Methanosarcina thermophila. Biochemistry37, 10027–10039.10.1021/bi9726483Search in Google Scholar PubMed

Staples, C.R., Ameyibor, E., Fu, W., Gardet-Salvi, L., Stritt-Etter, A.L., Schürmann, P., Knaff, D.B., and Johnson, M.K. (1996). The function and properties of the iron-sulfur center in spinach ferredoxin: thioredoxin reductase: a new biological role for iron-sulfur clusters. Biochemistry35, 11425–11434.10.1021/bi961007pSearch in Google Scholar PubMed

Staples, C.R., Gaymard, E., Stritt-Etter, A.L., Telser, J., Hoffman, B.M., Schürmann, P., Knaff, D.B., and Johnson, M.K. (1998). Role of the [Fe4-S4] cluster in mediating disulfide reduction in spinach ferredoxin:thioredoxin reductase. Biochemistry37, 4612–4620.10.1021/bi9729763Search in Google Scholar PubMed

Stojanowic, A., Mander, G.J., Duin, E.C., and Hedderich, R. (2003). Physiological role of the F420-non-reducing hydrogenase (Mvh) from Methanothermobacter marburgensis. Arch. Microbiol.180, 194–203.10.1007/s00203-003-0577-9Search in Google Scholar PubMed

Thauer, R.K. (1998). Biochemistry of methanogenesis: a tribute to Marjory Stephenson. Microbiology144, 2377–2406.Search in Google Scholar

Tietze, M., Beuchle, A., Lamla, I., Orth, N., Dehler, M., Greiner, G., and Beifuss, U. (2003). Redox potentials of methanophenazine and CoB-S-S-CoM, factors involved in electron transport in methanogenic archaea. ChemBioChem4, 333–335.10.1002/cbic.200390053Search in Google Scholar PubMed

Walters, E.M. and Johnson, M.K. (2004). Ferredoxin:thioredoxin reductase: disulfide reduction catalyzed via novel site-specific [4Fe-4S] cluster chemistry. Photosynth. Res.79, 249–264.10.1023/B:PRES.0000017195.05870.61Search in Google Scholar

Williams, C.H. (1995). Flavoprotein structure and mechanism. 6. Mechanism and structure of thioredoxin reductase from Escherichia coli. FASEB J.9, 1267–1276.Search in Google Scholar

Williams, C.H., Arscott, L.D., Muller, S., Lennon, B.W., Ludwig, M.L., Wang, P.F., Veine, D.M., Becker, K., and Schirmer, R.H. (2000). Thioredoxin reductase two modes of catalysis have evolved. Eur. J. Biochem.267, 6110–6117.10.1046/j.1432-1327.2000.01702.xSearch in Google Scholar PubMed

Published Online: 2005-10-12
Published in Print: 2005-10-01

©2005 by Walter de Gruyter Berlin New York

Downloaded on 12.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/BC.2005.112/html?lang=en
Scroll to top button