MetaCyc Pathway: sulfate reduction IV (dissimilatory)
Traceable author statement to experimental support

Enzyme View:

Pathway diagram: sulfate reduction IV (dissimilatory)

This view shows enzymes only for those organisms listed below, in the list of taxa known to possess the pathway. If an enzyme name is shown in bold, there is experimental evidence for this enzymatic activity.

Synonyms: sulfate respiration

Superclasses: Degradation/Utilization/AssimilationInorganic Nutrients MetabolismSulfur Compounds MetabolismSulfate Reduction
Generation of Precursor Metabolites and EnergyRespirationAnaerobic Respiration

Some taxa known to possess this pathway include : Archaeoglobus fulgidus, Archaeoglobus profundus, Bilophila wadsworthia RZATAU, Desulfotomaculum australicum, Desulfotomaculum geothermicum, Desulfotomaculum kuznetsovii, Desulfotomaculum nigrificans, Desulfovibrio desulfuricans, Desulfovibrio gigas, Desulfovibrio multispirans, Desulfovibrio sulfodismutans, Desulfovibrio vulgaris, Desulfovibrio vulgaris Hildenborough, Thermodesulfobacterium commune, Thermodesulforhabdus norvegica, Thermodesulfovibrio yellowstonii

Expected Taxonomic Range: Archaea, Bacteria

General Background

Sulfate is one of the most common electron acceptors for anaerobic respiration. Sulfate-reducing organisms are ubiquitous in anaerobic environments such as soil, sediments, marine and freshwaters, and the mouth and gut of many animals [Pires06]. Sulfate-reducers contribute greatly to the global cycling of carbon and sulfur, mostly in marine habitats, where the sulfate concentration is high. It is estimated that dissimilatory sulfate reduction is responsible for up to 50% of carbon remineralization in marine environments [Klenk97].

Dissimilatory sulfate-reducing prokaryotes are a heterogenous group of bacteria and archaea consisting of diverse phyla such as Archaeoglobi [Dahl01], Proteobacteria [Beeder95], Firmicutes [Daumas88], Nitrospirae [Henry94] and others that can use sulfate as a terminal electron acceptor. During the process, sulfate is ultimately reduced to hydrogen sulfide through the intermediates adenosine 5'-phosphosulfate (APS) and sulfite. The reduction of sulfate to sulfite requires two electrons at a standard redox potential (E0') of -516 mV, which is too high for physiological electron carriers [Thauer77]. This problem is solved by the formation of a mixed anhydride between the sulfate and phosphate, as in adenosine 5'-phosphosulfate (APS). This linkage lowers the potential to E0' = -60 mV, which is easilly negotiateded by biological reductants [Berndt04].

About This Pathway

All steps of sulfate reduction occur in the cytoplasm, implying that sulfate must be transported across the cytoplasmic membrane into the cell. Sulfate is activated with ATP in a reaction catalyzed by sulfate adenylyltransferase, resulting in the formation of adenosine 5'-phosphosulfate (APS) and pyrophosphate. This enzyme has an unfavorable equilibrium (Keq ~ 10-7 M) in the direction of APS formation, and it has been postulated that the reaction is driven by the hydrolysis of PPi by a ubiquitous inorganic pyrophosphatase [Segel87] and the favorable adenylylsulfate reductase reaction which consumes the product.

The next step is the reduction of APS to sulfite and AMP, which is catalyzed by adenylylsulfate reductase, for which the natural electron donor is not known.

The last enzyme in the pathway, dissimilatory sulfite reductase catalyzes the six-electron reduction of sulfite to sulfide, the main energy-conserving step in sulfate respiration. Dissimilatory sulfite reductases (DSRs) are present in all studied organisms capable of reducing sulfite to sulfide during anaerobic respiration. All DSR enzymes contain siroheme and [4Fe-4S] prosthetic centers, and they are classified according to their spectroscopic properties in four major groups which are: desulfoviridins (found in all Desulfovibrio strains [Lee71]), desulfurubidins (discovered in a mutant Desulfovibrio desulfuricans strain unable to synthethize desulfoviridin [Lee73]), desulfofuscidin (discovered in Thermodesulfobacterium commune [Hatchikian83]), and P582 (found in members of the Desulfotomaculum genus [Akagi73]).

The subunit structure was initially described as α2β2. Following the discovery of a third subunit, an α2β2γ2 structure was proposed for some organisms including Desulfovibrio vulgaris, Desulfovibrio gigas, Desulfovibrio desulfuricans [Pierik92] and Bilophila wadsworthia RZATAU [Laue01]. However, it is now accepted that the DsrC dimer is not a subunit of the sufite reductase, but rather a protein with which it interacts [Oliveira08].

A a mechanism for the process of sulfite reduction has been proposed: DsrAB persulfurates the DsrC sulfur carrier protein at one of its two conserved cysteine residues. DsrC then dissociates from the sulfite reductase, followed by the reduction of the persulfide by the second conserved cysteine. This results in release of hydrogen sulfide and the formation of an intramolecular disulfide in DsrC. Regeneration of the DsrC disulfide may be catalyzed by the DsrK DsrC-disulfide reductase subunit of the DsrMKJOP transmembrane complex (a membrane complex with disulfide/thiol reductase activity) [Oliveira08, Grein10].

Variants: sulfate reduction I (assimilatory), sulfate reduction II (assimilatory), sulfate reduction III (assimilatory), sulfate reduction V (dissimilatory)

Created 27-May-1999 by Pellegrini-Toole A, Marine Biological Laboratory
Revised 21-Sep-2006 by Caspi R, SRI International
Revised 10-Dec-2010 by Caspi R, SRI International


Akagi73: Akagi JM, Adams V (1973). "Isolation of a bisulfite reductase activity from Desulfotomaculum nigrificans and its identification as the carbon monoxide-binding pigment P582." J Bacteriol 116(1);392-6. PMID: 4745421

Beeder95: Beeder J, Torsvik T, Lien T (1995). "Thermodesulforhabdus norvegicus gen. nov., sp. nov., a novel thermophilic sulfate-reducing bacterium from oil field water." Arch Microbiol 164(5);331-6. PMID: 8572886

Berndt04: Berndt C, Lillig CH, Wollenberg M, Bill E, Mansilla MC, de Mendoza D, Seidler A, Schwenn JD (2004). "Characterization and reconstitution of a 4Fe-4S adenylyl sulfate/phosphoadenylyl sulfate reductase from Bacillus subtilis." J Biol Chem 279(9);7850-5. PMID: 14627706

Dahl01: Dahl C, Truper HG (2001). "Sulfite reductase and APS reductase from Archaeoglobus fulgidus." Methods Enzymol 331;427-41. PMID: 11265481

Daumas88: Daumas S, Cord-Ruwisch R, Garcia JL (1988). "Desulfotomaculum geothermicum sp. nov., a thermophilic, fatty acid-degrading, sulfate-reducing bacterium isolated with H2 from geothermal ground water." Antonie Van Leeuwenhoek 54(2);165-78. PMID: 3395110

Grein10: Grein F, Pereira IA, Dahl C (2010). "Biochemical Characterization of Individual Components of the Allochromatium vinosum DsrMKJOP Transmembrane Complex Aids Understanding of Complex Function In Vivo." J Bacteriol 192(24);6369-77. PMID: 20952577

Hatchikian83: Hatchikian EC, Zeikus JG (1983). "Characterization of a new type of dissimilatory sulfite reductase present in Thermodesulfobacterium commune." J Bacteriol 153(3);1211-20. PMID: 6826522

Henry94: Henry EA, Devereux R, Maki JS, Gilmour CC, Woese CR, Mandelco L, Schauder R, Remsen CC, Mitchell R (1994). "Characterization of a new thermophilic sulfate-reducing bacterium Thermodesulfovibrio yellowstonii, gen. nov. and sp. nov.: its phylogenetic relationship to Thermodesulfobacterium commune and their origins deep within the bacterial domain." Arch Microbiol 161(1);62-9. PMID: 11541228

Klenk97: Klenk HP, Clayton RA, Tomb JF, White O, Nelson KE, Ketchum KA, Dodson RJ, Gwinn M, Hickey EK, Peterson JD, Richardson DL, Kerlavage AR, Graham DE, Kyrpides NC, Fleischmann RD, Quackenbush J, Lee NH, Sutton GG, Gill S, Kirkness EF, Dougherty BA, McKenney K, Adams MD, Loftus B, Peterson S, Reich CI, McNeil LK, Badger JH, Glodek A, Zhou L, Overbeek R, Gocayne JD, Weidman JF, McDonald L, Utterback T, Cotton MD, Spriggs T, Artiach P, Kaine BP, Sykes SM, Sadow PW, D'Andrea KP, Bowman C, Fujii C, Garland SA, Mason TM, Olsen GJ, Fraser CM, Smith HO, Woese CR, Venter JC (1997). "The complete genome sequence of the hyperthermophilic, sulphate-reducing archaeon Archaeoglobus fulgidus." Nature 390(6658);364-70. PMID: 9389475

Laue01: Laue H, Friedrich M, Ruff J, Cook AM (2001). "Dissimilatory sulfite reductase (desulfoviridin) of the taurine-degrading, non-sulfate-reducing bacterium Bilophila wadsworthia RZATAU contains a fused DsrB-DsrD subunit." J Bacteriol 183(5);1727-33. PMID: 11160104

Lee71: Lee JP, Peck HD (1971). "Purification of the enzyme reducing bisulfite to trithionate from Desulfovibrio gigas and its identification as desulfoviridin." Biochem Biophys Res Commun 45(3);583-9. PMID: 5128167

Lee73: Lee JP, Yi CS, LeGall J, Peck HD (1973). "Isolation of a new pigment, desulforubidin, from Desulfovibrio desulfuricans (Norway strain) and its role in sulfite reduction." J Bacteriol 115(1);453-5. PMID: 4717523

Oliveira08: Oliveira TF, Vonrhein C, Matias PM, Venceslau SS, Pereira IA, Archer M (2008). "The crystal structure of Desulfovibrio vulgaris dissimilatory sulfite reductase bound to DsrC provides novel insights into the mechanism of sulfate respiration." J Biol Chem 283(49);34141-9. PMID: 18829451

Peck82: Peck HD, LeGall J (1982). "Biochemistry of dissimilatory sulphate reduction." Philos Trans R Soc Lond B Biol Sci 298(1093);443-66. PMID: 6127735

Pierik92: Pierik AJ, Duyvis MG, van Helvoort JM, Wolbert RB, Hagen WR (1992). "The third subunit of desulfoviridin-type dissimilatory sulfite reductases." Eur J Biochem 1992;205(1);111-5. PMID: 1555572

Pires06: Pires RH, Venceslau SS, Morais F, Teixeira M, Xavier AV, Pereira IA (2006). "Characterization of the Desulfovibrio desulfuricans ATCC 27774 DsrMKJOP complex--a membrane-bound redox complex involved in the sulfate respiratory pathway." Biochemistry 45(1);249-62. PMID: 16388601

Segel87: Segel IH, Renosto F, Seubert PA (1987). "Sulfate-activating enzymes." Methods Enzymol 143;334-49. PMID: 2821345

Thauer77: Thauer RK, Jungermann K, Decker K (1977). "Energy conservation in chemotrophic anaerobic bacteria." Bacteriol Rev 1977;41(1);100-80. PMID: 860983

Other References Related to Enzymes, Genes, Subpathways, and Substrates of this Pathway

Abola99: Abola AP, Willits MG, Wang RC, Long SR (1999). "Reduction of adenosine-5'-phosphosulfate instead of 3'-phosphoadenosine-5'-phosphosulfate in cysteine biosynthesis by Rhizobium meliloti and other members of the family Rhizobiaceae." J Bacteriol 181(17);5280-7. PMID: 10464198

Chen91a: Chen L, Liu MY, Le Gall J (1991). "Calcium is required for the reduction of sulfite from hydrogen in a reconstituted electron transfer chain from the sulfate reducing bacterium, Desulfovibrio gigas." Biochem Biophys Res Commun 1991;180(1);238-42. PMID: 1930220

Cort08: Cort JR, Selan U, Schulte A, Grimm F, Kennedy MA, Dahl C (2008). "Allochromatium vinosum DsrC: solution-state NMR structure, redox properties, and interaction with DsrEFH, a protein essential for purple sulfur bacterial sulfur oxidation." J Mol Biol 382(3);692-707. PMID: 18656485

Dahl90: Dahl, C., Koch, H., Keuken, O., Trueper, H.G. (1990). "Purification and characterization of ATP sulfurylase from the extremely thermophilic archaebacterial sulfate-reducer, Archaeoglobus fulgidus." FEMS Microbiol. Let. 67: 27-32.

Dahl93: Dahl C, Kredich NM, Deutzmann R, Truper HG (1993). "Dissimilatory sulphite reductase from Archaeoglobus fulgidus: physico-chemical properties of the enzyme and cloning, sequencing and analysis of the reductase genes." J Gen Microbiol 139(8);1817-28. PMID: 7691984

Frederiksen03: Frederiksen TM, Finster K (2003). "Sulfite-oxido-reductase is involved in the oxidation of sulfite in Desulfocapsa sulfoexigens during disproportionation of thiosulfate and elemental sulfur." Biodegradation 14(3);189-98. PMID: 12889609

Fritz00: Fritz G, Buchert T, Huber H, Stetter KO, Kroneck PM (2000). "Adenylylsulfate reductases from archaea and bacteria are 1:1 alphabeta-heterodimeric iron-sulfur flavoenzymes--high similarity of molecular properties emphasizes their central role in sulfur metabolism." FEBS Lett 473(1);63-6. PMID: 10802060

Fritz02: Fritz G, Roth A, Schiffer A, Buchert T, Bourenkov G, Bartunik HD, Huber H, Stetter KO, Kroneck PM, Ermler U (2002). "Structure of adenylylsulfate reductase from the hyperthermophilic Archaeoglobus fulgidus at 1.6-A resolution." Proc Natl Acad Sci U S A 99(4);1836-41. PMID: 11842205

Gavel98: Gavel OY, Bursakov SA, Calvete JJ, George GN, Moura JJ, Moura I (1998). "ATP sulfurylases from sulfate-reducing bacteria of the genus Desulfovibrio. A novel metalloprotein containing cobalt and zinc." Biochemistry 1998;37(46);16225-32. PMID: 9819214

Hansen94: Hansen TA (1994). "Metabolism of sulfate-reducing prokaryotes." Antonie Van Leeuwenhoek 1994;66(1-3);165-85. PMID: 7747930

Hatzfeld00: Hatzfeld Y, Lee S, Lee M, Leustek T, Saito K (2000). "Functional characterization of a gene encoding a fourth ATP sulfurylase isoform from Arabidopsis thaliana." Gene 2000;248(1-2);51-8. PMID: 10806350

Hawes73: Hawes CS, Nicholas DJ (1973). "Adenosine 5'-triphosphate sulphurylase from Saccharomyces cerevisiae." Biochem J 1973;133(3);541-50. PMID: 4582048

Higuchi87: Higuchi, Y.,, Inaka, K., Yasuoka, N., Yagi, T. (1987). "Isolation and crystallization of high molecular weight cytochrome from Desulfovibrio vulgaris Hildenborough." Biochim. Biophys. Acta 911:341-348.

Huang91: Huang CJ, Barrett EL (1991). "Sequence analysis and expression of the Salmonella typhimurium asr operon encoding production of hydrogen sulfide from sulfite." J Bacteriol 173(4);1544-53. PMID: 1704886

Jones74: Jones HE, Skyring GW (1974). "Reduction of sulphite to sulphide catalysed by desulfoviridin from Desulfovibrio gigas." Aust J Biol Sci 1974;27(1);7-14. PMID: 4824902

KarkhoffSchweiz95: Karkhoff-Schweizer RR, Huber DP, Voordouw G (1995). "Conservation of the genes for dissimilatory sulfite reductase from Desulfovibrio vulgaris and Archaeoglobus fulgidus allows their detection by PCR." Appl Environ Microbiol 61(1);290-6. PMID: 7887608

Kobayashi72: Kobayashi K, Takahashi E, Ishimoto M (1972). "Biochemical studies on sulfate-reducing bacteria. XI. Purification and some properties of sulfite reductase, desulfoviridin." J Biochem (Tokyo) 72(4);879-87. PMID: 4644321

Kraemer89: Kraemer, M., Cypionka, H. (1989). "Sulfate formation via ATP sulfurylase in thiosulfate- and sulfite-disproportionating bacteria." Arch. Microbiol. 151:232-237.

Lampreia90: Lampreia J, Moura I, Teixeira M, Peck HD, Legall J, Huynh BH, Moura JJ (1990). "The active centers of adenylylsulfate reductase from Desulfovibrio gigas. Characterization and spectroscopic studies." Eur J Biochem 1990;188(3);653-64. PMID: 2158885

Lampreia94: Lampreia J, Pereira AS, Moura JJG "Adenylylsulfate Reductases from Sulfate-Reducing Bacteria." Methods in Enzymology 243:241-260 (1994).

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Please cite the following article in publications resulting from the use of MetaCyc: Caspi et al, Nucleic Acids Research 42:D459-D471 2014
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