1887

Abstract

Green sulfur bacteria (GSB) oxidize sulfide and thiosulfate to sulfate, with extracellular globules of elemental sulfur as an intermediate. Here we investigated which genes are involved in the formation and consumption of these sulfur globules in the green sulfur bacterium . We show that sulfur globule oxidation is strictly dependent on the dissimilatory sulfite reductase (DSR) system. Deletion of /CT2244 or /CT2245, or the two clusters (CT0851–CT0854, CT2247–2250), abolished sulfur globule oxidation and prevented formation of sulfate from sulfide, whereas deletion of /CT2246 had no effect. The DSR system also seems to be involved in the formation of thiosulfate, because thiosulfate was released from wild-type cells during sulfide oxidation, but not from the mutants. The mutants incapable of complete substrate oxidation oxidized sulfide and thiosulfate about twice as fast as the wild-type, while having only slightly lower growth rates (70–80 % of wild-type). The increased oxidation rates seem to compensate for the incomplete substrate oxidation to satisfy the requirement for reducing equivalents during growth. A mutant in which two sulfide : quinone oxidoreductases (/CT0117 and /CT1087) were deleted exhibited a decreased sulfide oxidation rate (∼50 % of wild-type), yet formation and consumption of sulfur globules were not affected. The observation that mutants lacking the DSR system maintain efficient growth suggests that the DSR system is dispensable in environments with sufficiently high sulfide concentrations. Thus, the DSR system in GSB may have been acquired by horizontal gene transfer as a response to a need for enhanced substrate utilization in sulfide-limiting habitats.

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2011-04-01
2024-03-28
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References

  1. Azai C., Tsukatani Y., Harada J., Oh-oka H. 2009; Sulfur oxidation in mutants of the photosynthetic green sulfur bacterium Chlorobium tepidum devoid of cytochrome c -554 and SoxB. Photosynth Res 100:57–65
    [Google Scholar]
  2. Biebl H., Pfennig N. 1978; Growth yields of green sulfur bacteria in mixed cultures with sulfur and sulfate reducing bacteria. Arch Microbiol 117:9–16
    [Google Scholar]
  3. Brune D. C. 1989; Sulfur oxidation by phototrophic bacteria. Biochim Biophys Acta 975:189–221
    [Google Scholar]
  4. Chan L.-K., Morgan-Kiss R. M., Hanson T. E. 2008a; Genetic and proteomic studies of sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum . In Sulfur Metabolism in Phototrophic Organisms pp 357–373 Edited by Hell R., Dahl C., Knaff D. B., Leustek T. Dordrecht: Springer;
    [Google Scholar]
  5. Chan L.-K., Weber T. S., Morgan-Kiss R. M., Hanson T. E. 2008b; A genomic region required for phototrophic thiosulfate oxidation in the green sulfur bacterium Chlorobium tepidum (syn. Chlorobaculum tepidum . Microbiology 154:818–829
    [Google Scholar]
  6. Chan L.-K., Morgan-Kiss R. M., Hanson T. E. 2009; Functional analysis of three sulfide : quinone oxidoreductase homologs in Chlorobaculum tepidum . J Bacteriol 191:1026–1034
    [Google Scholar]
  7. Cline J. D. 1969; Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458
    [Google Scholar]
  8. Dahl C., Engels S., Pott-Sperling A. S., Schulte A., Sander J., Lübbe Y., Deuster O., Brune D. C. 2005; Novel genes of the dsr gene cluster and evidence for close interaction of Dsr proteins during sulfur oxidation in the phototrophic sulfur bacterium Allochromatium vinosum . J Bacteriol 187:1392–1404
    [Google Scholar]
  9. Eisen J. A., Nelson K. E., Paulsen I. T., Heidelberg J. F., Wu M., Dodson R. J., Deboy R., Gwinn M. L., Nelson W. C. other authors 2002; The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc Natl Acad Sci U S A 99:9509–9514
    [Google Scholar]
  10. Frigaard N.-U., Bryant D. A. 2001; Chromosomal gene inactivation in the green sulfur bacterium Chlorobium tepidum by natural transformation. Appl Environ Microbiol 67:2538–2544
    [Google Scholar]
  11. Frigaard N.-U., Bryant D. A. 2008; Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In Sulfur Metabolism in Phototrophic Organisms pp 337–355 Edited by Hell R., Dahl C., Knaff D. B., Leustek T. Dordrecht: Springer;
    [Google Scholar]
  12. Frigaard N.-U., Dahl C. 2009; Sulfur metabolism in phototrophic sulfur bacteria. In Advances in Microbial Physiology pp 103–200 Edited by Poole R. K. London: Academic Press;
    [Google Scholar]
  13. Frigaard N.-U., Chew A. G. M., Li H., Maresca J. A., Bryant D. A. 2003; Chlorobium tepidum : insights into the structure, physiology, and metabolism of a green sulfur bacterium derived from the complete genome sequence. Photosynth Res 78:93–117
    [Google Scholar]
  14. Frigaard N.-U., Sakuragi Y., Bryant D. A. 2004; Gene inactivation in the cyanobacterium Synechococcus sp. PCC 7002 and the green sulfur bacterium Chlorobium tepidum using in vitro-made DNA constructs and natural transformation. In Methods in Molecular Biology pp 325–340 Edited by Carpentier R. Totowa, NJ: Humana Press;
    [Google Scholar]
  15. Gibson J., Pfennig N., Waterbury J. B. 1984; Chloroherpeton thalassium gen. nov. et spec. nov ., a non-filamentous, flexing and gliding green sulfur bacterium. Arch Microbiol 138:96–101
    [Google Scholar]
  16. Grimm F., Cort J. R., Dahl C. 2010; DsrR, a novel IscA-like protein lacking iron- and Fe-S-binding functions, involved in the regulation of sulfur oxidation in Allochromatium vinosum . J Bacteriol 192:1652–1661
    [Google Scholar]
  17. Heunisch G. W. 1977; Stoichiometry of the reaction of sulfites with hydrogen sulfide ion. Inorg Chem 16:1411–1413
    [Google Scholar]
  18. Imhoff J. F. 2008; Systematics of anoxygenic phototrophic bacteria. In Sulfur Metabolism in Phototrophic Organisms pp 269–287 Edited by Hell R., Dahl C., Knaff D., Leustek T. Dordrecht: Springer;
    [Google Scholar]
  19. Jacobsen J. H., Rosgaard L., Sakuragi Y., Frigaard N.-U. 2011; One-step plasmid construction for generation of knock-out mutants in cyanobacteria: studies of glycogen metabolism in Synechococcus sp. PCC 7002. Photosynth Res 107:215–221
    [Google Scholar]
  20. Klein M., Friedrich M., Roger A. J., Hugenholtz P., Fishbain S., Abicht H., Blackall L. L., Stahl D. A., Wagner M. 2001; Multiple lateral transfers of dissimilatory sulfite reductase genes between major lineages of sulfate-reducing prokaryotes. J Bacteriol 183:6028–6035
    [Google Scholar]
  21. Kredich N. M. 1996; Biosynthesis of cysteine. In Escherichia coli and Salmonella, Cellular and Molecular Biology. pp 514–527 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  22. Lübbe Y. J., Youn H. S., Timkovich R., Dahl C. 2006; Siro(haem)amide in Allochromatium vinosum and relevance of DsrL and DsrN, a homolog of cobyrinic acid a , c -diamide synthase, for sulphur oxidation. FEMS Microbiol Lett 261:194–202
    [Google Scholar]
  23. Maresca J. A., Romberger S. P., Bryant D. A. 2008; Isorenieratene biosynthesis in green sulfur bacteria requires the cooperative actions of two carotenoid cyclases. J Bacteriol 190:6384–6391
    [Google Scholar]
  24. Meyer B., Imhoff J. F., Kuever J. 2007; Molecular analysis of the distribution and phylogeny of the soxB gene among sulfur-oxidizing bacteria – evolution of the Sox sulfur oxidation enzyme system. Environ Microbiol 9:2957–2977
    [Google Scholar]
  25. Mussmann M., Richter M., Lombardot T., Meyerdierks A., Kuever J., Kube M., Glöckner F. O., Amann R. 2005; Clustered genes related to sulfate respiration in uncultured prokaryotes support the theory of their concomitant horizontal transfer. J Bacteriol 187:7126–7137
    [Google Scholar]
  26. Ogawa T., Furusawa T., Nomura R., Seo D., Hosoya-Matsuda N., Sakurai H., Inoue K. 2008; SoxAX binding protein, a novel component of the thiosulfate-oxidizing multienzyme system in the green sulfur bacterium Chlorobium tepidum . J Bacteriol 190:6097–6110
    [Google Scholar]
  27. Overmann J. 2008; Ecology of phototrophic sulfur bacteria. In Sulfur Metabolism in Phototrophic Organisms pp 375–396 Edited by Hell R., Dahl C., Knaff D. B., Leustek T. Dordrecht: Springer;
    [Google Scholar]
  28. Pott A. S., 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. Microbiology 144:1881–1894
    [Google Scholar]
  29. Prange A., Chauvistré R., Modrow H., Hormes J., Trüper H. G., Dahl C. 2002; Quantitative speciation of sulfur in bacterial sulfur globules: X-ray absorption spectroscopy reveals at least three different species of sulfur. Microbiology 148:267–276
    [Google Scholar]
  30. Roy A. B., Trudinger P. A. 1970 The Biochemistry of Inorganic Compounds of Sulphur Cambridge, UK: Cambridge University Press;
    [Google Scholar]
  31. Sakurai H., Ogawa T., Shiga M., Inoue K. 2010; Inorganic sulfur oxidizing system in green sulfur bacteria. Photosynth Res 104:163–176
    [Google Scholar]
  32. Sander J., Engels-Schwarzlose S., Dahl C. 2006; Importance of the DsrMKJOP complex for sulfur oxidation in Allochromatium vinosum and phylogenetic analysis of related complexes in other prokaryotes. Arch Microbiol 186:357–366
    [Google Scholar]
  33. Schübbe S., Williams T. J., Xie G., Kiss H. E., Brettin T. S., Martinez D., Ross C. A., Schüler D., Cox B. L. other authors 2009; Complete genome sequence of the chemolithoautotrophic marine magnetotactic coccus strain MC-1. Appl Environ Microbiol 75:4835–4852
    [Google Scholar]
  34. Stal L. J., van Gemerden H., Krumbein W. E. 1984; The simultaneous assay of chlorophyll and bacteriochlorophyll in natural microbial communities. J Microbiol Methods 2:295–306
    [Google Scholar]
  35. Stanier R. Y., Smith J. H. C. 1960; The chlorophylls of green bacteria. Biochim Biophys Acta 41:478–484
    [Google Scholar]
  36. Steinmetz M. A., Fischer U. 1982; Cytochromes of the green sulfur bacterium Chlorobium vibrioforme f. thiosulfatophilum . Purification, characterization and sulfur metabolism. Arch Microbiol 131:19–26
    [Google Scholar]
  37. Steudel R., Holdt G., Visscher P. T., Van Gemerden H. 1990; Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol 153:432–437
    [Google Scholar]
  38. Theissen U., Hoffmeister M., Grieshaber M., Martin W. 2003; Single eubacterial origin of eukaryotic sulfide : quinone oxidoreductase, a mitochondrial enzyme conserved from the early evolution of eukaryotes during anoxic and sulfidic times. Mol Biol Evol 20:1564–1574
    [Google Scholar]
  39. Trüper H. G., Lorenz C., Schedel M., Steinmetz M. A. 1988; Metabolism of thiosulfate in Chlorobium . In Green Photosynthetic Bacteria Edited by Olson J., Ormerod J. G., Amesz J., Stackebrandt E., Trüper H. G. pp 189–200 New York: Plenum Press;
    [Google Scholar]
  40. Van Gemerden H. 1986; Production of elemental sulfur by green and purple sulfur bacteria. Arch Microbiol 146:52–56
    [Google Scholar]
  41. Wahlund T. M., Woese C. R., Castenholz R. W., Madigan M. T. 1991; A thermophilic green sulfur bacterium from New Zealand hot springs, Chlorobium tepidum sp. nov. Arch Microbiol 156:81–90
    [Google Scholar]
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