1887

Abstract

Recent studies with have suggested that homologues of the heat-shock sigma factor, RpoH, may not be involved in the heat-shock response in this -proteobacterium. The genome of another -proteobacterium, , which is considered to be a representative of the Fe(III)-reducing that predominate in a diversity of subsurface environments, contains an homologue. Characterization of the homologue revealed that it was induced by a temperature shift from 30 °C to 42 °C and that an -deficient mutant was unable to grow at 42 °C. The predicted heat-shock genes, , , , and , were heat-shock inducible in an -dependent manner, and comparison of promoter regions of these genes identified the consensus sequences for the −10 and −35 promoter elements. In addition, DNA elements identical to the CIRCE consensus sequence were found in promoters of , and , suggesting that these genes are regulated by a homologue of the repressor HrcA, which is known to bind the CIRCE element. These results suggest that the RpoH homologue is the heat-shock sigma factor and that heat-shock response in is regulated positively by RpoH as well as negatively by the HrcA/CIRCE system.

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2007-03-01
2024-10-08
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References

  1. Arrigo A. P., Iandry J. 1994 The Biology of Heat Shock Proteins and Molecular Chaperones Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  2. Bond D. R., Lovley D. R. 2003; Electricity production by Geobacter sulfurreducens attached to electrodes. Appl Environ Microbiol 69:1548–1555 [CrossRef]
    [Google Scholar]
  3. Bond D. R., Holmes D. E., Tender L. M., Lovley D. R. 2002; Electrode-reducing microorganisms that harvest energy from marine sediments. Science 295:483–485 [CrossRef]
    [Google Scholar]
  4. Caccavo F. Jr, Lonergan D. J., Lovley D. R., Davis M., Stolz J. F., McInerney M. J. 1994; Geobacter sulfurreducens sp. nov., a hydrogen- and acetate-oxidizing dissimilatory metal-reducing microorganism. Appl Environ Microbiol 60:3752–3759
    [Google Scholar]
  5. Chhabra S. R., He Q., Huang K. H., Gaucher S. P., Alm E. J., He Z., Hadi M. Z., Hazen T. C., Wall J. D. & other authors 2006; Global analysis of heat shock response in Desulfovibrio vulgaris Hidenborough. J Bacteriol 188:1817–1828 [CrossRef]
    [Google Scholar]
  6. Coppi M. V., Leang C., Sandler S. J., Lovley D. R. 2001; Development of a genetic system for Geobacter sulfurreducens . Appl Environ Microbiol 67:3180–3187 [CrossRef]
    [Google Scholar]
  7. Gross C. A. 1996; Function and regulation of the heat shock proteins. In Escherichia coli and Salmonella: Cellular and Molecular Biology , 2nd edn. pp 1382–1399 Edited by Neidhardt F. C. and others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  8. Hanahan D. 1983; Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166:557–580 [CrossRef]
    [Google Scholar]
  9. Harley C. B., Reynolds R. P. 1987; Analysis of E. coli promoter sequences. Nucleic Acids Res 15:2343–2361 [CrossRef]
    [Google Scholar]
  10. Hawley D. K., McClure W. R. 1983; Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res 11:2237–2255 [CrossRef]
    [Google Scholar]
  11. Hecker M., Schumann W., Volker U. 1996; Heat-shock and stress response in Bacillus subtilis . Mol Microbiol 19:417–428 [CrossRef]
    [Google Scholar]
  12. Hengge-Aronis R. 2002; Recent insights into the general stress response regulatory network in Escherichia coli . J Mol Microbiol Biotechnol 4:341–346
    [Google Scholar]
  13. Kovach M. E., Phillips R. W., Elzer P. H., Roop R. M., Peterson K. M. II 1994; pBBR1MCS: a broad-host-range cloning vector. BioTechniques 16:800–802
    [Google Scholar]
  14. Lindquist S., Craig E. A. 1998; The heat-shock proteins. Annu Rev Genet 22:631–677
    [Google Scholar]
  15. Lloyd J. R., Lovley D. R. 2001; Microbial detoxification of metals and radionuclides. Curr Opin Biotechnol 12:248–253 [CrossRef]
    [Google Scholar]
  16. Lovley D. R. 1997; Microbial Fe(III) reduction in subsurface environments. FEMS Microbial Rev 20:305–313 [CrossRef]
    [Google Scholar]
  17. Lovley D. R. 2003; Cleaning up with genomics: applying molecular biology to bioremediation. Nat Rev Microbiol 1:35–44 [CrossRef]
    [Google Scholar]
  18. Lovley D. R. 2006a; Microbial fuel cells: novel microbial physiologies and engineering approaches. Curr Opin Biotechnol 17:327–332 [CrossRef]
    [Google Scholar]
  19. Lovley D. R. 2006b; Bug juice: harvesting electricity with microorganisms. Nat Rev Microbiol 4:497–508 [CrossRef]
    [Google Scholar]
  20. Lovley D. R., Coates J. D. 1997; Bioremediation of metal contamination. Curr Opin Biotechnol 8:285–289 [CrossRef]
    [Google Scholar]
  21. Lovley D. R., Coates J. D. 2000; Novel forms of anaerobic respiration of environmental relevance. Curr Opin Microbiol 3:252–256 [CrossRef]
    [Google Scholar]
  22. Lovley D. R., Holmes D. E., Nevin K. P. 2004; Dissimilatory Fe(III) and Mn(IV) reduction. Adv Microb Physiol 49:219–286
    [Google Scholar]
  23. Marx C. J., Lidstrom M. E. 2001; Development of improved versatile broad-host-range vectors for use in methylotrophs and other Gram-negative bacteria. Microbiology 147:2065–2075
    [Google Scholar]
  24. Methé B. A., Nelson K. E., Eisen J. A., Paulsen I. T., Nelson W., Heidelberg J. F., Wu D., Wu M., Ward N. & other authors 2003; Genome of Geobacter sulfurreducens : metal reduction in subsurface environments. Science 302:1967–1969 [CrossRef]
    [Google Scholar]
  25. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  26. Mogk A., Homuth G., Scholz C., Kim L., Schmid F. X., Schumann W. 1997; The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis . EMBO J 16:4579–4590 [CrossRef]
    [Google Scholar]
  27. Nakahigashi K., Yanagi H., Yura T. 1995; Isolation and sequence analysis of rpoH genes encoding σ 32 from gram negative bacteria: conserved mRNA and protein segments for heat shock regulation. Nucleic Acids Res 23:4384–4390
    [Google Scholar]
  28. Nakahigashi K., Ron E. Z., Yanagi H., Yura T. 1999; Differential and independent roles of a σ 32 homolog (RpoH) and an HrcA repressor in the heat shock response of Agrobacterium tumefaciens . J Bacteriol 181:7509–7515
    [Google Scholar]
  29. Narberhaus F. 1999; Negative regulation of bacterial heat shock genes. Mol Microbiol 31:1–8 [CrossRef]
    [Google Scholar]
  30. Narberhaus F., Giebeler K., Bahl H. 1992; Molecular characterization of the dnaK gene region of Clostridium acetobutylicum , including grpE , dnaJ , and a new heat shock gene. J Bacteriol 174:3290–3299
    [Google Scholar]
  31. Narberhaus F., Krummenacher P., Fischer H. M., Hennecke H. 1997; Three disparately regulated genes for σ 32–like transcription factors in Bradyrhizobium japonicum . Mol Microbiol 24:93–104 [CrossRef]
    [Google Scholar]
  32. Núñez C., Adams L., Childers S., Lovley D. R. 2004; The RpoS sigma factor in the dissimilatory Fe(III)-reducing bacterium Geobacter sulfurreducens . J Bacteriol 186:5543–5546 [CrossRef]
    [Google Scholar]
  33. Reisenauer A., Mohr C. D., Shapiro L. 1996; Regulation of the heat shock σ 32 homolog in Caulobacter crescentus . J Bacteriol 178:1919–1927
    [Google Scholar]
  34. Riggs D. L., Cox M. B., Cheung-Flynn J., Prapapanich V., Carrigan P. E., Smith D. F. 2004; Functional specificity of co-chaperone interactions with Hsp90 client proteins. Crit Rev Biochem Mol Biol 39:279–295 [CrossRef]
    [Google Scholar]
  35. Roberts R. C., Toochinda C., Avedissian M., Baldini R. L., Gomes S. L., Shapiro L. 1996; Identification of a Caulobacter crescentus operon encoding hrcA , involved in negatively regulating heat-inducible transcription, and the chaperone gene grpE . J Bacteriol 178:1829–1841
    [Google Scholar]
  36. Rodionov D. A., Dubchak I., Arkin A., Alm E., Gelfand M. S. 2004; Reconstruction of regulatory and metabolic pathways in metal-reducing δ -proteobacteria. Genome Biol 5:R90 [CrossRef]
    [Google Scholar]
  37. Rosen R., Ron E. Z. 2002; Proteome analysis in the study of the bacterial heat-shock response. Mass Spectrom Rev 21:244–265 [CrossRef]
    [Google Scholar]
  38. Sandler S. J., Clark A. J. 1994; RecOR suppression of recF mutant phenotypes in Escherichia coli K-12. J Bacteriol 176:3661–3672
    [Google Scholar]
  39. Schulz A., Schumann W. 1996; hrcA , the first gene of the Bacillus subtilis dnaK operon encodes a negative regulator of class I heat shock genes. J Bacteriol 178:1088–1093
    [Google Scholar]
  40. Schumann W. 2000; Function and regulation of temperature-inducible bacterial proteins on the cellular metabolism. Adv Biochem Eng Biotechnol 67:1–33
    [Google Scholar]
  41. Schumann W. 2003; The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 8:207–217 [CrossRef]
    [Google Scholar]
  42. Servant P., Mazodier P. 2001; Negative regulation of the heat shock response in Streptomyces . Arch Microbiol 176:237–242 [CrossRef]
    [Google Scholar]
  43. Spohn G., Danielli A., Roncarati D., Delany I., Rappuoli R., Scarlato V. 2004; Dual control of Helicobacter pylori heat shock gene transcription by HspR and HrcA. J Bacteriol 186:2956–2965 [CrossRef]
    [Google Scholar]
  44. Taylor W. E., Straus D. B., Grossman A. D., Burton Z. F., Gross C. A., Burgess R. R. 1984; Transcription from a heat-inducible promoter causes heat shock regulation of the sigma subunit of E. coli RNA polymerase. Cell 38:371–381 [CrossRef]
    [Google Scholar]
  45. Ueki T., Inouye S. 2001; SigB, SigC, and SigE from Myxococcus xanthus homologues to sigma 32 are not required for heat shock response but for multicellular differentiation. J Mol Microbiol Biotechnol 3:287–293
    [Google Scholar]
  46. Ueki T., Inouye S. 2002; Transcriptional activation of a heat-shock gene, lonD , of Myxococcus xanthus by a two component histidine-aspartate phosphorelay system. J Biol Chem 277:6170–6177 [CrossRef]
    [Google Scholar]
  47. Ueki T., Inouye S. 2005; Identification of a gene involved in polysaccharide export as a transcription target of FruA, an essential factor for Myxococcus xanthus development. J Biol Chem 280:32279–32284 [CrossRef]
    [Google Scholar]
  48. Wetzstein M., Volker U., Dedio J., Lobau S., Zuber U., Schiesswohl M., Herget C., Hecker M., Schumann W. 1992; Cloning, sequencing, and molecular analysis of the dnaK locus from Bacillus subtilis . J Bacteriol 174:3300–3310
    [Google Scholar]
  49. Wu J., Newton A. 1996; Isolation, identification, and transcriptional specificity of the heat shock sigma factor σ 32 from Caulobacter crescentus . J Bacteriol 178:2094–2101
    [Google Scholar]
  50. Yan B., Ueki T., Puljic M., Adkins R. M., Lovley D. R., Krushkal J., Núñez C., Esteve-Núñez A., Methé B. A. 2006; Computational prediction of RpoS and RpoD regulatory sites in Geobacter sulfurreducens using sequence and gene expression information. Gene 384:73–95 [CrossRef]
    [Google Scholar]
  51. Young J. C., Agashe V. R., Siegers K., Hartl F. U. 2004; Pathways of chaperone-mediated protein folding in the cytosol. Nat Rev Mol Cell Biol 5:781–791 [CrossRef]
    [Google Scholar]
  52. Yura T., Kanemori M., Morita M. T. 2000; The heat shock response: regulation and function. In Bacterial Stress Responses pp 3–18 Edited by Storz G. Hengge-Aronis R. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  53. Zhang X., Beuron F., Freemont P. S. 2002; Machinery of protein folding and unfolding. Curr Opin Struct Biol 12:231–238 [CrossRef]
    [Google Scholar]
  54. Zuber U., Schumann W. 1994; CIRCE, a novel heat-shock element involved in regulation of heat-shock operon dnaK of Bacillus subtilis . J Bacteriol 176:1359–1363
    [Google Scholar]
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