1887

Abstract

To identify the actual substrate of the glutathione-dependent sulfur dioxygenase (EC 1.13.11.18) elemental sulfur oxidation of the meso-acidophilic strains DSM 504 and K6, strain R1 and DSM 700 was analysed. Extraordinarily high specific sulfur dioxygenase activities up to 460 nmol min (mg protein) were found in crude extracts. All cell-free systems oxidized elemental sulfur only via glutathione persulfide (GSSH), a non-enzymic reaction product from glutathione (GSH) and elemental sulfur. Thus, GSH plays a catalytic role in elemental sulfur activation, but is not consumed during enzymic sulfane sulfur oxidation. Sulfite is the first product of sulfur dioxygenase activity; it further reacted non-enzymically to sulfate, thiosulfate or glutathione -sulfonate (). Free sulfide was not oxidized by the sulfur dioxygenase. Persulfide as sulfur donor could not be replaced by other sulfane-sulfur-containing compounds (thiosulfate, polythionates, bisorganyl-polysulfanes or monoarylthiosulfonates). The oxidation of HS by the dioxygenase required GSSG, i.e. the disulfide of GSH, which reacted non-enzymically with sulfide to give GSSH prior to enzymic oxidation. On the basis of these results and previous findings a biochemical model for elemental sulfur and sulfide oxidation in and spp. is proposed.

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2003-07-01
2024-03-28
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References

  1. Anonymous 1984 Deutsche Einheitsverfahren zur Wasser-, Abwasser- und Schlammuntersuchung (DEV) Weinheim: VCH-Verlagsgesellschaft;
    [Google Scholar]
  2. Bradford M. M. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein, utilising the principle of protein-dye binding. Anal Biochem 72:248–254
    [Google Scholar]
  3. Buonfiglio V., Polidoro M., Flora L., Citro G., Valenti P., Orsi N. 1993; Identification of two outer membrane proteins involved in the oxidation of sulphur compounds in Thiobacillus ferrooxidans . FEMS Microbiol Rev 11:43–50
    [Google Scholar]
  4. Buonfiglio V., Polidoro M., Soyer F., Valenti P., Shively J. 1999; A novel gene encoding a sulfur-regulated outer membrane protein in Thiobacillus ferrooxidans . J Biotechnol 72:85–93
    [Google Scholar]
  5. Chahal B. S. 1986 A further study on the purification of the sulfur-oxidizing enzyme from Thiobacillus thiooxidans MSc thesis, University of Manitoba; Winnipeg, Canada:
    [Google Scholar]
  6. Chan C. W., Suzuki I. 1993; Quantitative extraction and determination of elemental sulfur and stoichiometric oxidation of sulfide to elemental sulfur by Thiobacillus ferrooxidans . Can J Microbiol 39:1166–1168
    [Google Scholar]
  7. de Jong G. A. H., Tang J. A., Bos P., de Vries S., Kuenen J. G. 2000; Purification and characterization of a sulfite : cytochrome c oxidoreductase from Thiobacillus acidophilus . J Mol Catal B 8:61–67
    [Google Scholar]
  8. Ehrlich H. L. 2002 Geomicrobiology New York: Marcel Dekker;
    [Google Scholar]
  9. Emmel T., Sand W., König W. A., Bock E. 1986; Evidence for the existence of a sulphur oxygenase in Sulfolobus brierleyi . J Gen Microbiol 132:3415–3420
    [Google Scholar]
  10. Fehér F. 1975; Schwefel, Selen, Tellur. In Handbuch der Präparativen Anorganischen Chemie vol. 1 pp  356–441 Edited by Brauer G. Stuttgart: Enke;
    [Google Scholar]
  11. Friedrich C. G., Rother D., Bradischewsky F., Quentmeier A., Fischer J. 2001; Oxidation of reduced inorganic sulfur compounds by bacteria: emergence of a common mechanism?. Appl Environ Microbiol 67:2873–2882
    [Google Scholar]
  12. Göbel T. 1988 Synthese und Analyse von kettenförmigen Polyschwefelver bindungen: Modelluntersuchungen zum Stoffwechsel der Schwefelbakterien PhD thesis, Technische Universität Berlin; Germany:
    [Google Scholar]
  13. Griesbeck C., Schütz M., Schödl T., Bathe S., Nausch L., Mederer N., Vielreicher M., Hauska G. 2002; Mechanism of sulfide-quinone reductase investigated using site-directed mutagenesis and sulfur analysis. Biochemistry 41:11552–11565
    [Google Scholar]
  14. Hallberg K. B., Thomson H. E. C., Boeselt I., Johnson D. B. 2001; Aerobic and anaerobic sulfur metabolism by acidophilic bacteria. In Biohydrometallurgy: Fundamentals, Technology and Sustainable Development. Process Metallurgy vol. 11A pp  423–431 Edited by Ciminelli V. S. T., Garcia O. Jr Amsterdam: Elsevier;
    [Google Scholar]
  15. Harrison A. P. Jr 1981; Acidiphilium cryptum gen. nov., sp. nov., heterotrophic bacterium from acidic mineral environments. Int J Syst Bacteriol 31:327–332
    [Google Scholar]
  16. Harrison A. P. Jr 1983; Genomic and physiological comparisons between heterotrophic thiobacilli and Acidiphilium cryptum , Thiobacillus versutus sp. nov., and Thiobacillus acidophilus nom. rev. Int J Syst Bacteriol 33:211–217
    [Google Scholar]
  17. Harrison A. P. Jr 1984; The acidophilic thiobacilli and other acidophilic bacteria that share their habitat. Annu Rev Microbiol 38:265–292
    [Google Scholar]
  18. He Z., Li Y., Zhou P., Liu S. 2000; Cloning and heterologous expression of a sulfur oxygenase/reductase gene from the thermoacidophilic archaeon Acidianus sp.S5 in Escherichia coli . FEMS Microbiol Lett 193:217–221
    [Google Scholar]
  19. Hipp W. M., Pott A. S., Thum-Schmitz N., Faath I., Dahl C., Trüper H. G. 1997; Towards the phylogeny of APS reductases and sirohaem sulfite reductases in sulfate-reducing and sulfur-oxidizing prokaryotes. Microbiology 143:2891–2902
    [Google Scholar]
  20. Hippe H. 2000; Leptospirillum gen. nov. (ex Markosyan 1972), nom. rev., including Leptospirillum ferrooxidans sp. nov. (ex Markosyan 1972), nom. rev, and Leptospirillum thermoferrooxidans sp. nov. (Golovacheva et al. 1992). Int J Syst Evol Microbiol 50:501–503
    [Google Scholar]
  21. Hiraishi A., Nagashima K. V. P., Matsuura K., Shimada K., Takaichi S., Wakao N., Katayama Y. 1998; Phylogeny and photosynthetic features of Thiobacillus acidophilus and related acidophilic bacteria: its transfer to the genus Acidiphilium as Acidiphilium acidophilum comb. nov. Int J Syst Bacteriol 48:1389–1398
    [Google Scholar]
  22. Kelly D. P. 1999; Thermodynamic aspects of energy conservation by chemolithotrophic sulfur bacteria in relation to the sulfur oxidation pathways. Arch Microbiol 171:219–229
    [Google Scholar]
  23. Kelly D. P., Wood A. P. 2000; Reclassification of some species of Thiobacillus to the newly designated genera Acidithiobacillus gen.nov., Halothiobacillus gen. nov. and Thermithiobacillus . Int J Syst Evol Microbiol 50:511–516
    [Google Scholar]
  24. Kletzin A. 1989; Coupled enzymatic production of sulfite, thiosulfate, and hydrogen sulfide from sulfur: purification and properties of a sulfur oxygenase reductase from the facultatively anaerobic archaebacterium Desulfurolobus ambivalens . J Bacteriol 171:1638–1643
    [Google Scholar]
  25. Kletzin A. 1992; Molecular characterization of the sor gene, which encodes the sulfur oxygenase/reductase of the thermoacidophilic archaeum Desulfurolobus ambivalens . J Bacteriol 174:5854–5859
    [Google Scholar]
  26. Krasil'nikova E. N., Bogdanova T. I., Zakharchuk L. M., Tsaplina I. A., Karavaiko G. I. 1998; Metabolism of reduced sulfur compounds in Sulfobacillus thermosufidooxidans , strain 1269. Mikrobiologiya 67:156–164 in Russian)
    [Google Scholar]
  27. Lens P. N. L., Hulshof Pol L. (editors) 2000 Environmental Technologies to Treat Sulfur Pollution London: IWA Publishing;
    [Google Scholar]
  28. Mackintosh M. E. 1978; Nitrogen fixation by Thiobacillus ferrooxidans . J Gen Microbiol 105:215–218
    [Google Scholar]
  29. Milde K., Sand W., Wolf W., Bock E. 1983; Thiobacilli of the corroded concrete walls of the Hamburg sewer system. J Gen Microbiol 129:1327–1333
    [Google Scholar]
  30. Moriarty D. J. W., Nicholas D. J. D. 1969; Enzymic sulphide oxidation of Thiobacillus concretivorus . Biochim Biophys Acta 184:114–123
    [Google Scholar]
  31. Moriarty D. J. W., Nicholas D. J. D. 1970; Products of sulphide oxidation in extracts of Thiobacillus concretivorus . Biochim Biophys Acta 197:143–151
    [Google Scholar]
  32. Nakamura K., Yoshikawa H., Okubo S., Kurosawa H., Amano Y. 1995; Purification and properties of membrane-bound sulfite dehydrogenase from Thiobacillus thiooxidans JCM 7814. Biosci Biotechnol Biochem 59:11–15
    [Google Scholar]
  33. Nübel T., Klughammer C., Huber R., Hauska G., Schütz M. 2000; Sulfide : quinone oxidoreductase in membranes of the hyperthermophilic bacterium Aquifex aeolicus (VF5). Arch Microbiol 173:233–244
    [Google Scholar]
  34. Ohmura N., Tsugita K., Koizumi J., Saiki H. 1996; Sulfur-binding protein of flagella of Thiobacillus ferrooxidans . J Bacteriol 178:5776–5780
    [Google Scholar]
  35. Parker C. D., Prisk J. 1953; The oxidation of inorganic compounds of sulphur by various sulphur bacteria. J Gen Microbiol 8:344–364
    [Google Scholar]
  36. Pott A. S., Dahl C. 1998; Siroheme sulfite reductase and other proteins encoded by genes at the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology 144:1881–1894
    [Google Scholar]
  37. Pronk J. T., Meulenberg R., Hazeu W., Bos P., Kuenen J. G. 1990; Oxidation of reduced inorganic sulphur compounds by acidophilic thiobacilli. FEMS Microbiol Rev 75:293–306
    [Google Scholar]
  38. Rawlings D. E. 2002; Heavy metal mining using microbes. Annu Rev Microbiol 56:65–91
    [Google Scholar]
  39. Rohwerder T., Jozsa P.-G., Gehrke T., Sand W. 2002; Bioleaching. In Encyclopedia of Environmental Microbiology vol 2 pp  632–641 Edited by Bitton G. New York: Wiley;
    [Google Scholar]
  40. Rother D., Henrich H.-J., Quentmeier A., Bradischewsky F., Friedrich C. G. 2001; Novel genes of the sox gene cluster, mutagenesis of the flavoprotein SoxF, and evidence for a general sulfur-oxidizing system in Paracoccus pantotrophus GB17. J Bacteriol 183:4499–4508
    [Google Scholar]
  41. Sand W., Rohde K., Sobotke B., Zenneck C. 1992; Evaluation of Leptospirillum ferrooxidans for leaching. Appl Environ Microbiol 58:85–92
    [Google Scholar]
  42. Schedel M., Trüper H. G. 1979; Purification of Thiobacillus denitrificans siroheme sulfite reductase and investigation of some molecular and catalytic properties. Biochim Biophys Acta 568:454–467
    [Google Scholar]
  43. Schippers A., Jørgensen B. B. 2001; Oxidation of pyrite and iron sulfide by manganese dioxide in marine sediments. Geochim Cosmochim Acta 65:915–922
    [Google Scholar]
  44. Silver M., Lundgren D. G. 1968; Sulfur-oxidizing enzyme of Ferrobacillus ferrooxidans ( Thiobacillus ferrooxidans ). Can J Biochem 46:457–461
    [Google Scholar]
  45. Spector T. 1978; Refinement of coomassie-blue method of protein quantitation. Anal Biochem 86:142–146
    [Google Scholar]
  46. Steudel R. 1996; Mechanism for the formation of elemental sulfur from aqueous sulfide in chemical and microbiological desulfurization processes. Ind Eng Chem Res 35:1417–1423
    [Google Scholar]
  47. Steudel R. 2000; The chemical sulfur cycle. In Environmental Technologies to Treat Sulfur Pollution . pp  1–31 Edited by Lens P. N. L., Hulshof Pol L. London: IWA Publishing;
  48. Steudel R., Albertsen A. 1992; Sulphur compounds CLVII. Determination of cysteine- S -sulphonate by ion pair chromatography and its formation by autoxidation of cysteine persulphide. J Chromatogr 606:260–263
    [Google Scholar]
  49. Steudel R., Kustos M. 1994; Sulfur: organic polysulfanes. In Encyclopedia of Inorganic Chemistry vol. 7 pp  4009–4038 Edited by King R. B. Chichester: Wiley;
    [Google Scholar]
  50. Sugio T., Mizunashi W., Inagaki K., Tano T. 1987; Purification and some properties of sulfur : ferric ion oxidoreductase from Thiobacillus ferrooxidans . J Bacteriol 169:4916–4922
    [Google Scholar]
  51. Sugio T., Katagiri T., Inagaki K., Tano T. 1989; Actual substrate for elemental sulfur oxidation by sulfur : ferric ion oxidoreductase purified from Thiobacillus ferrooxidans . Biochim Biophys Acta 973:250–256
    [Google Scholar]
  52. Sugio T., Suzuki H., Oto A., Inagaki K., Tanaka H., Tano T. 1991; Purification and some properties of a hydrogen sulfide-binding protein that is involved in sulfur oxidation of Thiobacillus ferrooxidans . Agric Biol Chem 55:2091–2097
    [Google Scholar]
  53. Sugio T., White K. J., Shute E. A., Choate D., Blake R. C. II 1992; Existence of a hydrogen sulfide : ferric ion oxidoreductase in iron-oxidizing bacteria. Appl Environ Microbiol 58:431–433
    [Google Scholar]
  54. Sugio T., Uemura S., Makino I., Iwahori K., Tano T., Blake R. C. II 1994; Sensitivity of iron-oxidizing bacteria, Thiobacillus ferrooxidans and Leptospirillum ferrooxidans , to bisulfite ion. Appl Environ Microbiol 60:722–725
    [Google Scholar]
  55. Suzuki I. 1965a; Oxidation of elemental sulfur by an enzyme system of Thiobacillus thiooxidans . Biochim Biophys Acta 104:359–371
    [Google Scholar]
  56. Suzuki I. 1965b; Incorporation of atmospheric oxygen-18 into thiosulfate by the sulfur-oxidizing enzyme of Thiobacillus thiooxidans . Biochim Biophys Acta 110:97–101
    [Google Scholar]
  57. Suzuki I. 1994; Sulfur-oxidizing enzymes. Methods Enzymol 243:455–462
    [Google Scholar]
  58. Suzuki I., Silver M. 1966; The initial product and properties of the sulfur-oxidizing enzyme of thiobacilli. Biochim Biophys Acta 122:22–33
    [Google Scholar]
  59. Vestal J. R., Lundgren D. G. 1971; The sulfite oxidase of Thiobacillus ferrooxidans ( Ferrobacillus ferrooxidans ). Can J Biochem 49:1125–1130
    [Google Scholar]
  60. Weiß J. 1991 Ionenchromatographie Weinheim: VCH;
    [Google Scholar]
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