1887

Abstract

Sulfur globules are formed as obligatory intermediates during the oxidation of reduced sulfur compounds in many environmentally important photo- and chemolithoautotrophic bacteria. It is well established that the so-called Dsr proteins are essential for the oxidation of zero-valent sulfur accumulated in the globules; however, hardly anything is known about the regulation of gene expression. Here, we present a closer look at the regulation of the genes in the phototrophic sulfur bacterium . The genes are expressed in a reduced sulfur compound-dependent manner and neither sulfite, the product of the reverse-acting dissimilatory sulfite reductase DsrAB, nor the alternative electron donor malate inhibit the gene expression. Moreover, we show the oxidation of sulfur to sulfite to be the rate-limiting step in the oxidation of sulfur to sulfate as sulfate production starts concomitantly with the upregulation of the expression of the genes. Real-time RT-PCR experiments suggest that the genes and are additionally expressed from secondary internal promoters, pointing to a special function of the encoded proteins. Earlier structural analyses indicated the presence of a helix–turn–helix (HTH)-like motif in DsrC. We therefore assessed the DNA-binding capability of the protein and provide evidence for a possible regulatory function of DsrC.

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2010-03-01
2020-10-22
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References

  1. Beller H. R., Chain P. S. G., Letain T. E., Chakicherla A., Larimer F. W., Richardson P. M., Coleman M. A., Wood A. P., Kelly D. P.. 2006a; The genome sequence of the obligately chemolithoautotrophic, facultatively anaerobic bacterium Thiobacillus denitrificans. J Bacteriol188:1473–1488
    [Google Scholar]
  2. Beller H. R., Letain T. E., Chakicherla A., Kane S. R., Legler T. C., Coleman M. A.. 2006b; Whole-genome transcriptional analysis of chemolithoautotrophic thiosulfate oxidation by Thiobacillus denitrificans under aerobic versus denitrifying conditions. J Bacteriol188:7005–7015
    [Google Scholar]
  3. Bradford M. M.. 1976; A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem72:248–254
    [Google Scholar]
  4. Chan L.-K., Morgan-Kiss R., Hanson T. E.. 2008a; Sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum): genetic and proteomic analyses. In Microbial Sulfur Metabolism pp117–126 Edited by Dahl C., Friedrich C. G.. Heidelberg & Berlin: Springer;
  5. Chan L.-K., Morgan-Kiss R., Hanson T. E.. 2008b; Genetic and proteomic studies of sulfur oxidation in Chlorobium tepidum (syn. Chlorobaculum tepidum. In Sulfur Metabolism in Phototrophic Organisms pp357–373 Edited by Hell R., Dahl C., Knaff D. B., Leustek T.. Dordrecht: Springer;
  6. Cort J. R., Mariappan S. V. S., Kim C.-Y., Park M. S., Peat T. S., Waldo G. S., Terwilliger T. C., Kennedy M. A.. 2001; Solution structure of Pyrobaculum aerophilum DsrC, an archaeal homologue of the gamma subunit of dissimilatory sulfite reductase. Eur J Biochem268:5842–5850
    [Google Scholar]
  7. Cort J. R., Selan U., Schulte A., Grimm F., Kennedy M. A., 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 Biol382:692–707
    [Google Scholar]
  8. Dahl C.. 1996; Insertional gene inactivation in a phototrophic sulphur bacterium: APS-reductase-deficient mutants of Chromatium vinosum. Microbiology142:3363–3372
    [Google Scholar]
  9. Dahl C.. 2008; Inorganic sulfur compounds as electron donors in purple sulfur bacteria. In Sulfur Metabolism in Phototrophic Organisms pp289–317 Edited by Hell R., Dahl C., Knaff D. B., Leustek T.. Dordrecht: Springer;
  10. Dahl C., Prange A.. 2006; Bacterial sulfur globules: occurrence, structure and metabolism. In Inclusions in Prokaryotes pp21–51 Edited by Shively J. M.. Heidelberg: Springer;
  11. 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 Bacteriol187:1392–1404
    [Google Scholar]
  12. Dahl C., Schulte A., Stockdreher Y., Hong C., Grimm F., Sander J., Kim R., Kim S.-H., Shin D. H.. 2008; Structural and molecular genetic insight into a widespread sulfur oxidation pathway. J Mol Biol384:1287–1300
    [Google Scholar]
  13. 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 A99:9509–9514
    [Google Scholar]
  14. Fey A., Eichler S., Flavier S., Christen R., Höfle M. G., Guzmán C. A.. 2004; Establishment of a real-time PCR-based approach for accurate quantification of bacterial RNA targets in water, using Salmonella as a model organism. Appl Environ Microbiol70:3618–3623
    [Google Scholar]
  15. Frigaard N.-U., Bryant D. A.. 2008; Genomic insights into the sulfur metabolism of phototrophic green sulfur bacteria. In Sulfur Metabolism in Phototrophic Organisms pp337–355 Edited by Hell R., Dahl C., Knaff D. B., Leustek T.. Dordrecht: Springer;
  16. Frigaard N.-U., Dahl C.. 2009; Sulfur metabolism in phototrophic sulfur bacteria. Adv Microb Physiol54:103–200
    [Google Scholar]
  17. Fuller R. C., Smillie R. M., Sisler E. C., Kronberg H. L.. 1961; Carbon metabolism in Chromatium. J Biol Chem236:2140–2149
    [Google Scholar]
  18. Grimm F., Franz B., Dahl C.. 2008; Thiosulfate and sulfur oxidation in purple sulfur bacteria. In Microbial Sulfur Metabolism pp101–116 Edited by Dahl C., Friedrich C. G.. Berlin & Heidelberg: Springer;
  19. Haveman S. A., Brunelle V., Voordouw J. K., Voordouw G., Heidelberg J. F., Rabus R.. 2003; Gene expression analysis of energy metabolism mutants of Desulfovibrio vulgaris Hildenborough indicates an important role for alcohol dehydrogenase. J Bacteriol185:4345–4353
    [Google Scholar]
  20. Hübner P., Willison J. C., Vignais P., Bickle T. A.. 1991; Expression of regulatory nif genes in Rhodobacter capsulatus. J Bacteriol173:2993–2999
    [Google Scholar]
  21. Hurlbert R. E.. 1968; Effect of thiol-binding reagents on the metabolism of Chromatium D. J Bacteriol95:1706–1712
    [Google Scholar]
  22. Hurlbert R. E., Lascelles J.. 1963; Ribulose diphosphate carboxylase in Thiorhodaceae. J Gen Microbiol33:445–458
    [Google Scholar]
  23. Imhoff J. F.. 2003; Phylogenetic taxonomy of the family Chlorobiaceae on the basis of 16S rRNA and fmo (Fenna–Matthews–Olson protein) gene sequences. Int J Syst Evol Microbiol53:941–951
    [Google Scholar]
  24. Kappler U., Dahl C.. 2001; Enzymology and molecular biology of prokaryotic sulfite oxidation. FEMS Microbiol Lett203:1–9
    [Google Scholar]
  25. Karkhoff-Schweizer R. R., Bruschi M., Voordouw G.. 1993; Expression of the γ-subunit gene of desulfoviridin-type dissimilatory sulfite reductase and of the α- and β-subunit genes is not coordinately regulated. Eur J Biochem211:501–507
    [Google Scholar]
  26. Lee Y.-H., Nadaraia S., Gu D., Becker D. F., Tanner J. J.. 2003; Structure of the proline dehydrogenase domain of the multifunctional PutA flavoprotein. Nat Struct Biol10:109–114
    [Google Scholar]
  27. Loy A., Duller S., Baranyi C., Mußmann M., Ott J., Sharon I., Béjà O., Le Paslier D., Dahl C., Wagner M.. 2009; Reverse dissimilatory sulfite reductase as phylogenetic marker for a subgroup of sulfur-oxidizing prokaryotes. Environ Microbiol11:289–299
    [Google Scholar]
  28. 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 Lett261:194–202
    [Google Scholar]
  29. Miller J. H.. 1972; Assay of β-galactosidase. In Experiments in Molecular Genetics pp352–355 Edited by Miller J. H.. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  30. Numata T., Fukai S., Ikeuchi Y., Suzuki T., Nureki O.. 2006; Structural basis for sulfur relay to RNA mediated by heterohexameric TusBCD complex. Structure14:357–366
    [Google Scholar]
  31. Oliveira T. F., Vonrhein C., Matia P. M., Venceslau S. S., Pereira I. A. C., 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 Chem283:34141–34149
    [Google Scholar]
  32. Pattaragulwanit K., Dahl C.. 1995; Development of a genetic system for a purple sulfur bacterium: conjugative plasmid transfer in Chromatium vinosum. Arch Microbiol164:217–222
    [Google Scholar]
  33. Pfennig N., Trüper H. G.. 1989; Anoxygenic phototrophic bacteria. In Bergey's Manual of Systematic Bacteriologyvol. 3 pp1635–1653 Edited by Staley J. T., Bryant M. P., Pfennig N., Holt J. G.. Baltimore: Williams & Wilkins;
  34. Pott A. S., Dahl C.. 1998; Sirohaem sulfite reductase and other proteins encoded in the dsr locus of Chromatium vinosum are involved in the oxidation of intracellular sulfur. Microbiology144:1881–1894
    [Google Scholar]
  35. Prange A., Engelhardt H., Trüper H. G., Dahl C.. 2004; The role of the sulfur globule proteins of Allochromatium vinosum: mutagenesis of the sulfur globule protein genes and expression studies by real-time RT PCR. Arch Microbiol182:165–174
    [Google Scholar]
  36. Roof D. M., Roth J. R.. 1992; Autogenous regulation of ethanolamine utilization by a transcriptional activator of the eut operon in Salmonella typhimurium. J Bacteriol174:6634–6643
    [Google Scholar]
  37. Sahl H. G., Trüper H. G.. 1977; Enzymes of CO2 fixation in Chromatiaceae. FEMS Microbiol Lett2:129–132
    [Google Scholar]
  38. Sander J., Dahl C.. 2009; Metabolism of inorganic sulfur compounds in purple bacteria. In The Purple Phototrophic Bacteria pp595–622 Edited by Hunter C. N., Daldal F., Thurnauer M. C., Beatty J. T. Dordrecht: Springer;
  39. 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 Microbiol186:357–366
    [Google Scholar]
  40. Schäfer A., Tauch A., Jäger W., Kalinowski J., Thierbach G., Pühler A.. 1994; Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene145:69–73
    [Google Scholar]
  41. Schedel M., Trüper H. G.. 1979; Purification of Thiobacillus denitrificans siroheme sulfite reductase and investigation of some molecular and catalytic properties. Biochim Biophys Acta568:454–467
    [Google Scholar]
  42. Schedel M., Vanselow M., Trüper H. G.. 1979; Siroheme sulfite reductase isolated from Chromatium vinosum. Purification and investigation of some of its molecular and catalytic properties. Arch Microbiol121:29–36
    [Google Scholar]
  43. Steudel R., Holdt G., Visscher P. T., van Gemerden H.. 1990; Search for polythionates in cultures of Chromatium vinosum after sulfide incubation. Arch Microbiol153:432–437
    [Google Scholar]
  44. Wek R. C., Hatfield G. W.. 1986; Examination of the internal promoter, PE, in the ilvGMEDA operon of E. coli K-12. Nucleic Acids Res14:2763–2777
    [Google Scholar]
  45. White C. E., Winans S. C.. 2007; The quorum-sensing transcription factor TraR decodes its DNA binding site by direct contacts with DNA bases and by detection of DNA flexibility. Mol Microbiol64:245–256
    [Google Scholar]
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