MetaCyc Pathway: sulfite oxidation III
Traceable author statement to experimental support

Enzyme View:

Pathway diagram: sulfite oxidation III

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.

Superclasses: Degradation/Utilization/AssimilationInorganic Nutrients MetabolismSulfur Compounds MetabolismSulfite Oxidation

Some taxa known to possess this pathway include : Allochromatium vinosum, Chlorobium limicola, endosymbiont of Riftia pachyptila, Thiobacillus denitrificans, Thiobacillus thioparus, Thiocapsa roseopersicina

Expected Taxonomic Range: Bacteria

General Background

Sulfite plays a key role in oxidative sulfur metabolism. It can derived from multiple sources: first, sulfite is the main intermediate in the oxidation of sulfur compounds to sulfate [Kappler01]. In purple sulfur bacteria such as Allochromatium vinosum, the oxidation of hydrogen sulfide and thiosulfate results in formation of intracellular sulfur globules, which are oxidized to sulfite by the Dsr system (see superpathway of sulfide oxidation (phototrophic sulfur bacteria)).

A second source for sulfite is the desulfonation of organic compounds by enzymes like EC, sulfoacetaldehyde acetyltransferase (Xsc) (see sulfoacetaldehyde degradation I).

A third source is extracellular sulfite retrieved from the environment. Free sulfite in the periplasm (which most likely exists as hydrogen sulfite) is bound to the SoxYZ protein complex in the form of [a SoxY protein]-L-cysteine-S-sulfinate. The binding acts to shield components of the periplasm from chemical reactions with sulfite, and may also be required for delivering the sulfite to a transporter that exports it into the cytoplasm for oxidation [Dahl13]. Some microorganisms (such as Sulfitobacter species) can use sulfite as their sole electron source [Sorokin95, Pukall99].

Enzymes that catalyze the direct oxidation of sulfite to sulfate are molybdenum hydroxylases, and belong to the sulfite oxidase family, which includes both sulfite-oxidizing enzymes and plant assimilatory nitrate reductases (such as the sulfite oxidase of Arabidopsis thaliana col). The best characterized members of this family are sulfite oxidases from avian and mammalian sources. However, these enzymes differ from the bacterial enzymes in that they can use oxygen as an electron acceptor (see EC, sulfite oxidase).

Some sulfite oxidizing enzyme are located in the periplasm. The best characterized enzyme from this group is sulfite dehydrogenase (SOR) from Starkeya novella, which contains a molybdopyranopterin cofactor (see sulfite oxidation I (sulfite oxidoreductase)). Another well-characterized periplasmic enzyme is the Sox enzyme system (such as that from Paracoccus pantotrophus). It has been shown that this system can oxidize sulfite in vitro, but it is not clear whether it functions in vivo as a sulfite-oxidizing enzyme [Friedrich00a, Lu84, Friedrich01a]).

Other enzyme systems that oxidize sulfite are located in the cytoplasm. Two general mechanisms for sulfite oxidation in the cytoplasm have been described: a direct oxidation by a membrane-bound iron-sulfur molybdoprotein (this pathway) and an indirect, AMP-dependent oxidation via the intermediate adenosine 5'-phosphosulfate (APS) (see sulfite oxidation II and sulfite oxidation III) [Kappler01]. The direct oxidation route is much more prevalent, but the two mechanisms are present simultaneously in many organisms, including β and γ proteobacteria ( Thiobacillus thioparus, Allochromatium vinosum, Thiobacillus denitrificans, Beggiatoa), green sulfur bacteria ( Chlorobium), Gram-positive bacteria ( Sulfobacillus thermosulfidooxidans) and even archaea ( Acidianus ambivalens) [Kappler01].

While many organisms possess only the direct mechanism, the only examples for organisms that possess only the non-direct mechanism are found in the bacterial endosymbionts of invertebrates [Nelson95].

About This Pathway

Two variations are known for the non-direct sulfite oxidation pathway. Both variations share the same first step, the AMP-dependent oxidation of sulfite to adenosine 5'-phosphosulfate, which is catalyzed by the enzyme APS reductase. The pathways differ in the second step. In one variation (depicted here) the AMP moiety of APS is transferred to diphosphate by dissimilatory sulfate adenylyltransferase, generating sulfate and ATP, while in the other variation the AMP-moiety is transfered to phosphate by the enzyme adenylylsulfate:phosphate adenylyltransferase (APAT), generating sulfate and ADP (see sulfite oxidation II). The APS pathways can operate in both directions (see sulfate reduction IV (dissimilatory)), and were discovered originally in sulfate-reducing organisms [Peck62]. When operating in sulfite oxidation mode, they result in substrate level phosphorylation, and may provide the bacteria with energy [Peck68].

The oxidation of sulfite by the indirect pathway occurs in the cytoplasm. The first enzyme of the pathway, APS reductase, has been described as either a soluble enzyme, or a membrane bound enzyme. The other enzymes are soluble [Kappler01]. Even though the enzyme dissimilatory sulfate adenylyltransferase has only been isolated from few sulfur-oxidizers (but many sulfate-reducers), this pathway has been demonstrated in several slfur-oxidizing bacteria, including Allochromatium vinosum [Neumann00], Chlorobium limicola, Thiocapsa roseopersicina, Thiobacillus thioparus, and Thiobacillus denitrificans ( [Sanchez01, Hipp97, Kappler01] and references therein).

Superpathways: superpathway of sulfur metabolism (Desulfocapsa sulfoexigens), superpathway of thiosulfate metabolism (Desulfovibrio sulfodismutans), superpathway of sulfide oxidation (phototrophic sulfur bacteria)

Variants: sulfite oxidation I (sulfite oxidoreductase), sulfite oxidation II, sulfite oxidation IV, sulfite oxidation V (SoeABC)

Created 09-Aug-2006 by Caspi R, SRI International


Bagchi05: Bagchi A, Ghosh TC (2005). "A structural study towards the understanding of the interactions of SoxY, SoxZ, and SoxB, leading to the oxidation of sulfur anions via the novel global sulfur oxidizing (sox) operon." Biochem Biophys Res Commun 335(2);609-15. PMID: 16084835

Dahl13: Dahl C, Franz B, Hensen D, Kesselheim A, Zigann R (2013). "Sulfite oxidation in the purple sulfur bacterium Allochromatium vinosum: identification of SoeABC as a major player and relevance of SoxYZ in the process." Microbiology 159(Pt 12);2626-38. PMID: 24030319

Friedrich00a: Friedrich CG, Quentmeier A, Bardischewsky F, Rother D, Kraft R, Kostka S, Prinz H (2000). "Novel genes coding for lithotrophic sulfur oxidation of Paracoccus pantotrophus GB17." J Bacteriol 182(17);4677-87. PMID: 10940005

Friedrich01a: Friedrich CG, Rother D, Bardischewsky F, Quentmeier A, Fischer J (2001). "Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?." Appl Environ Microbiol 67(7);2873-82. PMID: 11425697

Hipp97: Hipp WM, Pott AS, Thum-Schmitz N, Faath I, Dahl C, Truper HG (1997). "Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes." Microbiology 143 ( Pt 9);2891-902. PMID: 9308173

Kappler01: Kappler U, Dahl C (2001). "Enzymology and molecular biology of prokaryotic sulfite oxidation." FEMS Microbiol Lett 203(1);1-9. PMID: 11557133

Lu84: Lu, W.P., Kelly, D.P. (1984). "Properties and role of sulphite:cytochrome c oxidoreductase purified from Thiobacillus versutus (A2)." J. Gen. Microbiol. 130(7):1683-1692.

Nelson95: Nelson, D.C., Hagen, K.D. (1995). "Physiology and biochemistry of symbiotic and free-living chemoautotrophic sulfur bacteria." Am. Zool. 35: 91-101.

Neumann00: Neumann S, Wynen A, Truper HG, Dahl C (2000). "Characterization of the cys gene locus from Allochromatium vinosum indicates an unusual sulfate assimilation pathway." Mol Biol Rep 27(1);27-33. PMID: 10939523

Peck62: Peck, H.D. (1962). "Symposium on metabolism of inorganic compounds. V. Comparative metabolism of inorganic sulfur compounds in microorganisms." Bacteriol Rev 26;67-94. PMID: 14484819

Peck68: Peck HD (1968). "Energy-coupling mechanisms in chemolithotrophic bacteria." Annu Rev Microbiol 22;489-518. PMID: 4972376

Pukall99: Pukall R, Buntefuss D, Fruhling A, Rohde M, Kroppenstedt RM, Burghardt J, Lebaron P, Bernard L, Stackebrandt E (1999). "Sulfitobacter mediterraneus sp. nov., a new sulfite-oxidizing member of the alpha-Proteobacteria." Int J Syst Bacteriol 49 Pt 2;513-9. PMID: 10319472

Quentmeier01: Quentmeier A, Friedrich CG (2001). "The cysteine residue of the SoxY protein as the active site of protein-bound sulfur oxidation of Paracoccus pantotrophus GB17." FEBS Lett 503(2-3);168-72. PMID: 11513876

Quentmeier03: Quentmeier A, Hellwig P, Bardischewsky F, Grelle G, Kraft R, Friedrich CG (2003). "Sulfur oxidation in Paracoccus pantotrophus: interaction of the sulfur-binding protein SoxYZ with the dimanganese SoxB protein." Biochem Biophys Res Commun 312(4);1011-8. PMID: 14651972

Sanchez01: Sanchez O, Ferrera I, Dahl C, Mas J (2001). "In vivo role of adenosine-5'-phosphosulfate reductase in the purple sulfur bacterium Allochromatium vinosum." Arch Microbiol 176(4);301-5. PMID: 11685375

Sorokin95: Sorokin, D.Y. (1995). "Sulfitobacter pontiacus gen. nov., sp. nov. - a new heterotrophic bacterium from the Black Sea, specialized on sulfite oxidation." Mikrobiologiya 64:354-365.

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

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

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.

Dahl96: Dahl C (1996). "Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum." Microbiology 142 ( Pt 12);3363-72. PMID: 9004500

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

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

Latendresse13: Latendresse M. (2013). "Computing Gibbs Free Energy of Compounds and Reactions in MetaCyc."

Laue94: Laue BE, Nelson DC (1994). "Characterization of the gene encoding the autotrophic ATP sulfurylase from the bacterial endosymbiont of the hydrothermal vent tubeworm Riftia pachyptila." J Bacteriol 176(12);3723-9. PMID: 8206850

Leustek94: Leustek T, Murillo M, Cervantes M (1994). "Cloning of a cDNA encoding ATP sulfurylase from Arabidopsis thaliana by functional expression in Saccharomyces cerevisiae." Plant Physiol 1994;105(3);897-902. PMID: 8058839

Leyh88: Leyh TS, Taylor JC, Markham GD (1988). "The sulfate activation locus of Escherichia coli K12: cloning, genetic, and enzymatic characterization." J Biol Chem 263(5);2409-16. PMID: 2828368

Liu94a: Liu C, Martin E, Leyh TS (1994). "GTPase activation of ATP sulfurylase: the mechanism." Biochemistry 33(8);2042-7. PMID: 8117661

Logan96: Logan HM, Cathala N, Grignon C, Davidian JC (1996). "Cloning of a cDNA encoded by a member of the Arabidopsis thaliana ATP sulfurylase multigene family. Expression studies in yeast and in relation to plant sulfur nutrition." J Biol Chem 1996;271(21);12227-33. PMID: 8647819

Murillo95: Murillo M, Leustek T (1995). "Adenosine-5'-triphosphate-sulfurylase from Arabidopsis thaliana and Escherichia coli are functionally equivalent but structurally and kinetically divergent: nucleotide sequence of two adenosine-5'-triphosphate-sulfurylase cDNAs from Arabidopsis thaliana and analysis of a recombinant enzyme." Arch Biochem Biophys 1995;323(1);195-204. PMID: 7487067

Parey13: Parey K, Demmer U, Warkentin E, Wynen A, Ermler U, Dahl C (2013). "Structural, biochemical and genetic characterization of dissimilatory ATP sulfurylase from Allochromatium vinosum." PLoS One 8(9);e74707. PMID: 24073218

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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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