1887

Microbiology Society logo

Volume 148, Issue 2

Control of dimethylsulfoxide reductase expression in : the role of carbon metabolites and the response regulators DorR and RegA Free

Abstract

Regulation of the expression of dimethylsulfoxide (DMSO) reductase was investigated in the purple phototrophic bacterium . Under phototrophic, anaerobic conditions with malate as carbon source, DMSO caused an approximately 150-fold induction of DMSO reductase activity. The response regulator DorR was required for DMSO-dependent induction and also appeared to slightly repress DMSO reductase expression in the absence of substrate. Likewise, when pyruvate replaced malate as carbon source there was an induction of DMSO reductase activity in cells grown at low light intensity (16 W m) and again this induction was dependent on DorR. The level of DMSO reductase activity in aerobically grown cells was elevated when pyruvate replaced malate as carbon source. One possible explanation for this is that acetyl phosphate, produced from pyruvate, may activate expression of DMSO reductase by direct phosphorylation of DorR, leading to low levels of induction of gene expression in the absence of DMSO. A mutant lacking the global response regulator of photosynthesis gene expression, RegA, exhibited high levels of DMSO reductase in the absence of DMSO, when grown phototrophically with malate as carbon source. This suggests that phosphorylated RegA acts as a repressor of operon expression under these conditions. It has been proposed elsewhere that RegA-dependent expression is negatively regulated by the cytochrome oxidase. A mutant lacking cytochrome exhibited significantly higher levels of Φ[::] activity in the presence of DMSO compared to wild-type cells and this is consistent with the above model. Pyruvate restored DMSO reductase expression in the mutant to the same pattern as found in wild-type cells. These data suggest that contains a regulator of DMSO respiration that is distinct from DorR and RegA, is activated in the presence of pyruvate, and acts as a negative regulator of DMSO reductase expression.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): dimethylsulfoxide respiration , DMSO, dimethylsulfoxide , gene expression , ONP, o-nitrophenol , Rhodobacter capsulatus and TMAO, trimethylamine N-oxide
© Microbiology Society
Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-2-605
2002-02-01
2024-05-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/2/1480605a.html?itemId=/content/journal/micro/10.1099/00221287-148-2-605&mimeType=html&fmt=ahah

References

  1. Ansaldi M., Simon G., Lepelletier M., Mejean V. 2000; The TorR high-affinity binding site plays a key role in both torR autoregulation and torCAD operon expression in Escherichia coli . J Bacteriol 182:961–966 [CrossRef]
     [Google Scholar]
  2. Beringer J. E. 1974; R factor transfer in Rhizobium leguminosarum. J Gen Microbiol 84:188–198 [CrossRef]
     [Google Scholar]
  3. Bouché S., Klauck E., Fischer D., Lucassen M., Jung K., Hengge-Aronis R. 1998; Regulation of RssB-dependent proteolysis in Escherichia coli : a role for acetyl phosphate in a response regulator-controlled process. Mol Microbiol 27:787–795 [CrossRef]
     [Google Scholar]
  4. Bowman W. C., Du S., Bauer C. E., Kranz R. G. 1999; In vitro activation and repression of photosynthesis gene transcription in Rhodobacter capsulatus . Mol Microbiol 33:429–437 [CrossRef]
     [Google Scholar]
  5. Clark J. M., Switzer R. L. 1977 Experimental Biochemistry New York: W. H. Freeman;
     [Google Scholar]
  6. Cox J. C., Madigan M. T., Favinger J. L., Gest H. 1980; Redox mechanisms in ‘‘oxidant-dependent’’ hexose fermentation by Rhodopseudomonas capsulata . Arch Biochem Biophys 204:10–17 [CrossRef]
     [Google Scholar]
  7. Daldal F., Cheng C., Applebaum J., Davidson E., Prince R. C. 1986; Cytochrome c 2 is not essential for photosynthetic growth of Rhodopseudomonas capsulata . Proc Natl Acad Sci USA 83:2012–2016 [CrossRef]
     [Google Scholar]
  8. Du S. Y., Bird T. H., Bauer C. E. 1998; DNA binding characteristics of RegA* – a constitutively active anaerobic activator of photosynthesis gene expression in Rhodobacter capsulatus . J Biol Chem 273:18509–18513 [CrossRef]
     [Google Scholar]
  9. Elsen S., Dischert W., Colbeau A., Bauer C. E. 2000; Expression of uptake hydrogenase and molybdenum nitrogenase in Rhodobacter capsulatus is coregulated by the RegB-RegA two-component regulatory system. J Bacteriol 182:2831–2837 [CrossRef]
     [Google Scholar]
  10. Emmerich R., Hennecke H., Fischer H.-M. 2000a; Evidence for a functional similarity between the two-component regulatory systems RegSR, ActSR and RegAB (PrrAB) in α-Proteobacteria. Arch Microbiol 174:307–313 [CrossRef]
     [Google Scholar]
  11. Emmerich R., Strehler P., Hennecke H., Fischer H. M. 2000b; An imperfect inverted repeat is critical for DNA binding of the response regulator RegR of Bradyrhizobium japonicum . Nucleic Acids Res 28:4166–4171 [CrossRef]
     [Google Scholar]
  12. Hatton M. D., Malin G., McEwan A. G. 1994; Identification of a periplasmic dimethylsulfoxide reductase in Hyphomicrobium EG grown under chemolithoheterotrophic conditions with dimethylsulfoxide as carbon source. Arch Microbiol 162:148–150 [CrossRef]
     [Google Scholar]
  13. Hemschemeier S. K., Kirndorfer M., Hebermehl M., Klug G. 2000; DNA binding of wild type RegA protein and its differential effect on the expression of pigment binding proteins in Rhodobacter capsulatus . J Mol Microbiol Biotechnol 2:235–243
     [Google Scholar]
  14. Horne I. M., Pemberton J. M., McEwan A. G. 1996; Photosynthesis gene expression in Rhodobacter sphaeroides is regulated by redox changes which are linked to electron transport. Microbiology 142:2831–2838 [CrossRef]
     [Google Scholar]
  15. Koch H.-G., Hwang O., Daldal F. 1998; Isolation and characterization of Rhodobacter capsulatus mutants affected in cytochrome cbb 3 oxidase activity. J Bacteriol 180:969–978
     [Google Scholar]
  16. Madigan M. T., Gest H. 1978; Growth of a photosynthetic bacterium anaerobically in darkness supported by ‘‘oxidant-dependent’’ sugar fermentation. Arch Microbiol 117:119–122 [CrossRef]
     [Google Scholar]
  17. Madigan M. T., Gest H. 1979; Growth of the photosynthetic bacterium Rhodopseudomonas capsulata chemoautotrophically in darkness with H2 as the energy source. J Bacteriol 137:524–530
     [Google Scholar]
  18. Madigan M. T., Cox J. C., Gest H. 1980; Physiology of dark fermentative growth of Rhodopseudomonas capsulata . J Bacteriol 142:908–915
     [Google Scholar]
  19. McCleary W. R., Stock J. B. 1994; Acetyl phosphate and the activation of two-component response regulators. J Biol Chem269 31567–31572
     [Google Scholar]
  20. McEwan A. G., Wetzstein H. G., Ferguson S. J., Jackson J. B. 1985; Periplasmic location of the terminal oxidoreductase in trimethylamine-N-oxide and dimethylsulphoxide respiration in the photosynthetic bacterium Rhodopseudomonas capsulata . Biochim Biophys Acta 806:140–147
     [Google Scholar]
  21. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  22. Mouncey N., Kaplan S. 1998a; Redox-dependent gene regulation in Rhodobacter sphaeroides 2.4.1T: effects on dimethylsulfoxide reductase ( dor ) gene expression. J Bacteriol 180:5612–5618
     [Google Scholar]
  23. Mouncey N., Kaplan S. 1998b; Cascade regulation of dimethyl sulfoxide reductase (dor ) gene expression in the facultative phototroph Rhodobacter sphaeroides 2.4.1. J Bacteriol 180:2924–2930
     [Google Scholar]
  24. Mouncey N., Choudhary M., Kaplan S. 1997; Characterisation of the genes encoding dimethylsulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: an essential metabolic gene function encoded by chromosome II. J Bacteriol 179:7617–7624
     [Google Scholar]
  25. Nyström T. 1994; The glucose-starvation stimulon of Escherichia coli : induced and repressed synthesis of enzymes of central metabolic pathways and role of acetyl phosphate in gene expression and starvation survival. Mol Microbiol 12:833–843 [CrossRef]
     [Google Scholar]
  26. O’Gara J. P., Kaplan S. 1997; Evidence for the role of redox carriers in photosynthesis gene expression and carotenoid biosynthesis in Rhodobacter sphaeroides 2.4.1. J Bacteriol 179:1951–1961
     [Google Scholar]
  27. O’Gara J. P., Eraso J. M., Kaplan S. 1998; A redox-responsive pathway for aerobic regulation of photosynthesis gene expression in Rhodobacter spaeroides 2.4.1. J Bacteriol 180:4044–4050
     [Google Scholar]
  28. Oh J. I., Kaplan S. 1999; The cbb 3 terminal oxidase of Rhodobacter sphaeroides 2.4.1: structural and functional implications for the regulation of spectral complex formation. Biochemistry 38:2688–2696 [CrossRef]
     [Google Scholar]
  29. Oh J. I., Kaplan S. 2001; Generalized approach to the regulation and integration of gene expression. Mol Microbiol 39:1116–1123 [CrossRef]
     [Google Scholar]
  30. Prüß B. 1998; Acetyl phosphate and the phosphorylation of the OmpR are involved in the regulation of the cell division rate in Escherichia coli . Arch Microbiol 170:141–146 [CrossRef]
     [Google Scholar]
  31. Qian Y., Tabita F. R. 1996; A global signal transduction system regulates aerobic and anaerobic CO2 fixation in Rhodobacter sphaeroides . J Bacteriol 178:12–18
     [Google Scholar]
  32. Richardson D. J., King G. F., Kelly D. J., McEwan A. G., Ferguson S. J., Jackson J. B. 1988; The role of auxiliary oxidants in maintaining redox balance during phototrophic growth of Rhodobacter capsulatus on propionate or butyrate. Arch Microbiol 150:131–137 [CrossRef]
     [Google Scholar]
  33. Roh J. H., Kaplan S. 2000; Genetic and phenotypic analyses of the rdx locus of Rhodobacter sphaeroides 2.4.1. J Bacteriol 182:3475–3481 [CrossRef]
     [Google Scholar]
  34. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
     [Google Scholar]
  35. Schultz J. E., Weaver P. F. 1982; Fermentation anaerobic respiration by Rhodospirillum rubrum and Rhodopseudomonas capsulata . J Bacteriol 149:181–190
     [Google Scholar]
  36. Sganga M. W., Bauer C. E. 1992; Regulatory factors controlling photosynthetic reaction center and light-harvesting gene expression in Rhodobacter capsulatus . Cell 68:945–954 [CrossRef]
     [Google Scholar]
  37. Shaw A. L. 1998 Characterisation of the Rhodobacter capsulatus dimethylsulfoxide reductase (dor) operon PhD thesis The University of Queensland; Australia:
     [Google Scholar]
  38. Shaw A. L., Klipp W., Hanson G. R., McEwan A. G., Leimkühler S. 1999a; Mutational analysis of the dimethylsulfoxide respiratory ( dor ) operon of Rhodobacter capsulatus . Microbiology 145:1409–1420 [CrossRef]
     [Google Scholar]
  39. Shaw A. L., Hochkoeppler A., Bonora P., Zannoni D., Hanson G. R., McEwan A. G. 1999b; Characterization of DorC from Rhodobacter capsulatus , a c -type cytochrome involved in electron transfer to dimethyl sulfoxide reductase. J Biol Chem 274:9911–9914 [CrossRef]
     [Google Scholar]
  40. Simon G., Jourlin C., Ansaldi M., Pascal M., Chippaux M., Mejean V. 1995; Binding of the TorR regulator to cis -acting direct repeats activates tor operon expression. Mol Microbiol 17:971–980 [CrossRef]
     [Google Scholar]
  41. Simon R., Priefer U., Puhler A. 1983; A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram negative bacteria. Bio/Technology 1:784–791 [CrossRef]
     [Google Scholar]
  42. Solomon P. S., Shaw A. L., Lane I., Hanson G. R., Palmer T., McEwan A. G. 1999; Characterisation of a molybdenum cofactor biosynthetic gene cluster in Rhodobacter capsulatus which is specific for the biogenesis of dimethylsulfoxide reductase. Microbiology 145:1421–1429 [CrossRef]
     [Google Scholar]
  43. Solomon P. S., Shaw A. L., Young M. D., Hanson G. R., Klipp W., McEwan A. G., Leimkühler S. 2000; Molybdate-dependent expression of dimethylsulfoxide reductase in Rhodobacter capsulatus . FEMS Microbiol Lett 190:203–208 [CrossRef]
     [Google Scholar]
  44. Swem L. R., Elsen S., Bird T. E., Swem D. L., Koch H.-G., Myllikallio H., Dalda F., Bauer C. E. 2001; The RegB/RegA two component regulatory system controls synthesis of photosynthesis and respiratory electron transfer components in Rhodobacter capsulatus . J Mol Biol 309:121–138 [CrossRef]
     [Google Scholar]
  45. Ujiiye T., Yamamoto I., Satoh T. 1997; The dmsR gene encoding a dimethyl sulfoxide-responsive regulator for expression of dmsCBA (dimethyl sulfoxide respiration genes) in Rhodobacter sphaeroides f.sp. denitrificans . Biochim Biophys Acta 1353:84–92 [CrossRef]
     [Google Scholar]
  46. Wang G., Angermueller S., Klipp W. 1993; Characterization of Rhodobacter capsulatus genes encoding a molybdenum transport-system and putative molybdenum-pterin-binding-proteins. J Bacteriol 175:3031–3042
     [Google Scholar]
  47. Weaver P. F., Wall J. D., Gest H. 1975; Characterisation of Rhodopseudomonas capsulata. Arch Microbiol 105:207–216 [CrossRef]
     [Google Scholar]
  48. Yamamoto Y., Ujiye T., Ohshima Y., Satoh T. 2001; Mutational analysis of regulatory cis -acting elements for the transcriptional activation of the dmsCBA operon in Rhodobacter sphaeroides f.sp. denitrificans . Plant Cell Physiol 42:703–709 [CrossRef]
     [Google Scholar]
  49. Zannoni D. 1995; Aerobic and anaerobic transport chains in anoxygenic phototrophic bacteria. In Anoxygenic Photosynthetic Bacteria pp 949–971 Edited by Blankenship R. E., Madigan M. T., Bauer C. E. Dordrecht: Kluwer;
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-2-605
Loading
Control of dimethylsulfoxide reductase expression in Rhodobacter capsulatus: the role of carbon metabolites and the response regulators DorR and RegA
Microbiology 148, 605 (2002); https://doi.org/10.1099/00221287-148-2-605
/content/journal/micro/10.1099/00221287-148-2-605
/content/journal/micro/10.1099/00221287-148-2-605
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error