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Volume 157, Issue 1

Novel regulation modules of Gram-positive bacteria involve the use of complex hybrid histidine kinases Free

Abstract

A common bacterial strategy to cope with stressful conditions is the activation of alternative sigma factors that control specific regulons enabling targeted responses. In the human pathogen , activation of the major stress-responsive sigma factor is controlled by a signalling route that involves the multi-sensor hybrid histidine kinase RsbK. RsbK-type kinases are not restricted to the group, but occur in a wide variety of other bacterial species, including members of the the low-GC Gram-positive genera and as well as the high-GC actinobacteria. Genome context and protein sequence analyses of 118 RsbK homologues revealed extreme variability in N-terminal sensory as well as C-terminal regulatory domains and suggested that RsbK-type kinases are subject to complex fine-tuning systems, including sensitization and desensitization via methylation and demethylation within the helical domain preceding the H-box. The RsbK-mediated stress-responsive sigma factor activation mechanism that has evolved in and the other species differs markedly from the extensively studied and highly conserved RsbRST-mediated activation route found in and other low-GC Gram-positive bacteria. Implications for future research on sigma factor control mechanisms are presented and current knowledge gaps are briefly discussed.

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Keyword(s): HK, histidine kinase , MCP, methyl-accepting chemotaxis protein , REC, RR receiver , RR, response regulator and TCS, two-component signal transduction system
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2011-01-01
2024-04-27
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References

  1. Akbar S., Gaidenko T. A., Kang C. M., O'Reilly M., Devine K. M., Price C. W. 2001; New family of regulators in the environmental signaling pathway which activates the general stress transcription factor σ B of Bacillus subtilis . J Bacteriol 183:1329–1338
     [Google Scholar]
  2. Alm E., Huang K., Arkin A. 2006; The evolution of two-component systems in bacteria reveals different strategies for niche adaptation. PLOS Comput Biol 2:e143
     [Google Scholar]
  3. Anantharaman V., Balaji S., Aravind L. 2006; The signaling helix: a common functional theme in diverse signaling proteins. Biol Direct 1:25
     [Google Scholar]
  4. Ávila-Pérez M., Hellingwerf K. J., Kort R. 2006; Blue light activates the σ B-dependent stress response of Bacillus subtilis via YtvA. J Bacteriol 188:6411–6414
     [Google Scholar]
  5. Ávila-Pérez M., van der Steen J. B., Kort R., Hellingwerf K. J. 2010; Red light activates the σ B-mediated general stress response of Bacillus subtilis via the energy branch of the upstream signaling cascade. J Bacteriol 192:755–762
     [Google Scholar]
  6. Bishop A., Fielding S., Dyson P., Herron P. 2004; Systematic insertional mutagenesis of a streptomycete genome: a link between osmoadaptation and antibiotic production. Genome Res 14:893–900
     [Google Scholar]
  7. Brody M. S., Vijay K., Price C. W. 2001; Catalytic function of an α / β hydrolase is required for energy stress activation of the σ B transcription factor in Bacillus subtilis . J Bacteriol 183:6422–6428
     [Google Scholar]
  8. Brody M. S., Stewart V., Price C. W. 2009; Bypass suppression analysis maps the signalling pathway within a multidomain protein: the RsbP energy stress phosphatase 2C from Bacillus subtilis . Mol Microbiol 72:1221–1234
     [Google Scholar]
  9. Chaturongakul S., Raengpradub S., Wiedmann M., Boor K. J. 2008; Modulation of stress and virulence in Listeria monocytogenes . Trends Microbiol 16:388–396
     [Google Scholar]
  10. Chen C. C., Lewis R. J., Harris R., Yudkin M. D., Delumeau O. 2003; A supramolecular complex in the environmental stress signalling pathway of Bacillus subtilis . Mol Microbiol 49:1657–1669
     [Google Scholar]
  11. Chen C. C., Yudkin M. D., Delumeau O. 2004; Phosphorylation and RsbX-dependent dephosphorylation of RsbR in the RsbR-RsbS complex of Bacillus subtilis . J Bacteriol 186:6830–6836
     [Google Scholar]
  12. Cho Y. H., Lee E. J., Ahn B. E., Roe J. H. 2001; SigB, an RNA polymerase sigma factor required for osmoprotection and proper differentiation of Streptomyces coelicolor . Mol Microbiol 42:205–214
     [Google Scholar]
  13. Crooks G. E., Hon G., Chandonia J. M., Brenner S. E. 2004; WebLogo: a sequence logo generator. Genome Res 14:1188–1190
     [Google Scholar]
  14. Dandekar T., Snel B., Huynen M., Bork P. 1998; Conservation of gene order: a fingerprint of proteins that physically interact. Trends Biochem Sci 23:324–328
     [Google Scholar]
  15. de Been M., Francke C., Moezelaar R., Abee T., Siezen R. J. 2006; Comparative analysis of two-component signal transduction systems of Bacillus cereus , Bacillus thuringiensis and Bacillus anthracis . Microbiology 152:3035–3048
     [Google Scholar]
  16. de Been M., Tempelaars M. H., van Schaik W., Moezelaar R., Siezen R. J., Abee T. 2010; A novel hybrid kinase is essential for regulating the σ B-mediated stress response of Bacillus cereus . Environ Microbiol 12:730–745
     [Google Scholar]
  17. Delumeau O., Dutta S., Brigulla M., Kuhnke G., Hardwick S. W., Voelker U., Yudkin M. D., Lewis R. J. 2004; Functional and structural characterization of RsbU, a stress signaling protein phosphatase 2C. J Biol Chem 279:40927–40937
     [Google Scholar]
  18. Delumeau O., Chen C. C., Murray J. W., Yudkin M. D., Lewis R. J. 2006; High-molecular-weight complexes of RsbR and paralogues in the environmental signaling pathway of Bacillus subtilis . J Bacteriol 188:7885–7892
     [Google Scholar]
  19. Dufour A., Voelker U., Voelker A., Haldenwang W. G. 1996; Relative levels and fractionation properties of Bacillus subtilis σ B and its regulators during balanced growth and stress. J Bacteriol 178:3701–3709
     [Google Scholar]
  20. Fabret C., Feher V. A., Hoch J. A. 1999; Two-component signal transduction in Bacillus subtilis : how one organism sees its world. J Bacteriol 181:1975–1983
     [Google Scholar]
  21. Fernández Martínez L. F., Bishop A., Parkes L., Del Sol R., Salerno P., Sevcikova B., Mazurakova V., Kormanec J., Dyson P. 2009; Osmoregulation in Streptomyces coelicolor : modulation of SigB activity by OsaC. Mol Microbiol 71:1250–1262
     [Google Scholar]
  22. Fouet A., Namy O., Lambert G. 2000; Characterization of the operon encoding the alternative σ B factor from Bacillus anthracis and its role in virulence. J Bacteriol 182:5036–5045
     [Google Scholar]
  23. Gaidenko T. A., Kim T. J., Weigel A. L., Brody M. S., Price C. W. 2006; The blue-light receptor YtvA acts in the environmental stress signaling pathway of Bacillus subtilis . J Bacteriol 188:6387–6395
     [Google Scholar]
  24. Galperin M. Y. 2004; Bacterial signal transduction network in a genomic perspective. Environ Microbiol 6:552–567
     [Google Scholar]
  25. Grebe T. W., Stock J. B. 1999; The histidine protein kinase superfamily. Adv Microb Physiol 41:139–227
     [Google Scholar]
  26. Gruber T. M., Gross C. A. 2003; Multiple sigma subunits and the partitioning of bacterial transcription space. Annu Rev Microbiol 57:441–466
     [Google Scholar]
  27. Hazelbauer G. L., Lai W. C. 2010; Bacterial chemoreceptors: providing enhanced features to two-component signaling. Curr Opin Microbiol 13:124–132
     [Google Scholar]
  28. Hecker M., , Pané-Farré J., Voelker U. 2007; SigB-dependent general stress response in Bacillus subtilis and related gram-positive bacteria. Annu Rev Microbiol 61:215–236
     [Google Scholar]
  29. Hoch J. A. 2000; Two-component and phosphorelay signal transduction. Curr Opin Microbiol 3:165–170
     [Google Scholar]
  30. Hulko M., Berndt F., Gruber M., Linder J. U., Truffault V., Schultz A., Martin J., Schultz J. E., Lupas A. N., Coles M. 2006; The HAMP domain structure implies helix rotation in transmembrane signaling. Cell 126:929–940
     [Google Scholar]
  31. Kim T. J., Gaidenko T. A., Price C. W. 2004; A multicomponent protein complex mediates environmental stress signaling in Bacillus subtilis . J Mol Biol 341:135–150
     [Google Scholar]
  32. Lee E. J., Cho Y. H., Kim H. S., Ahn B. E., Roe J. H. 2004; Regulation of σ B by an anti- and an anti-anti-sigma factor in Streptomyces coelicolor in response to osmotic stress. J Bacteriol 186:8490–8498
     [Google Scholar]
  33. Lee E. J., Karoonuthaisiri N., Kim H. S., Park J. H., Cha C. J., Kao C. M., Roe J. H. 2005; A master regulator σ B governs osmotic and oxidative response as well as differentiation via a network of sigma factors in Streptomyces coelicolor . Mol Microbiol 57:1252–1264
     [Google Scholar]
  34. Le Moual H., Koshland D. E. Jr 1996; Molecular evolution of the C-terminal cytoplasmic domain of a superfamily of bacterial receptors involved in taxis. J Mol Biol 261:568–585
     [Google Scholar]
  35. Letunic I., Doerks T., Bork P. 2009; SMART 6: recent updates and new developments. Nucleic Acids Res 37:D229–D232
     [Google Scholar]
  36. Marles-Wright J., Grant T., Delumeau O., van Duinen G., Firbank S. J., Lewis P. J., Murray J. W., Newman J. A., Quin M. B. other authors 2008; Molecular architecture of the “stressosome,” a signal integration and transduction hub. Science 322:92–96
     [Google Scholar]
  37. McLachlan A. D., Stewart M. 1975; Tropomyosin coiled-coil interactions: evidence for an unstaggered structure. J Mol Biol 98:293–304
     [Google Scholar]
  38. Mittenhuber G. 2002; A phylogenomic study of the general stress response sigma factor σ B of Bacillus subtilis and its regulatory proteins. J Mol Microbiol Biotechnol 4:427–452
     [Google Scholar]
  39. Novick R. P. 2003; Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48:1429–1449
     [Google Scholar]
  40. Overbeek R., Fonstein M., D'Souza M., Pusch G. D., Maltsev N. 1999; The use of gene clusters to infer functional coupling. Proc Natl Acad Sci U S A 96:2896–2901
     [Google Scholar]
  41. Pané-Farré J., Lewis R. J., Stülke J. 2005; The RsbRST stress module in bacteria: a signalling system that may interact with different output modules. J Mol Microbiol Biotechnol 9:65–76
     [Google Scholar]
  42. Perez E., Zheng H., Stock A. M. 2006; Identification of methylation sites in Thermotoga maritima chemotaxis receptors. J Bacteriol 188:4093–4100
     [Google Scholar]
  43. Price C. W. 2002; General stress response. In Bacillus Subtilis and its Closest Relatives: from Genes to Cells pp 369–384 Edited by Sonenshein A. L., Hoch J. A., Losick R. Washington, DC: American Society for Microbiology;
     [Google Scholar]
  44. Shi X., Wegener-Feldbrügge S., Huntley S., Hamann N., Hedderich R., Søgaard-Andersen L. 2008; Bioinformatics and experimental analysis of proteins of two-component systems in Myxococcus xanthus . J Bacteriol 190:613–624
     [Google Scholar]
  45. van Schaik W., Abee T. 2005; The role of σ B in the stress response of Gram-positive bacteria – targets for food preservation and safety. Curr Opin Biotechnol 16:218–224
     [Google Scholar]
  46. van Schaik W., Tempelaars M. H., Zwietering M. H., de Vos W. M., Abee T. 2005; Analysis of the role of RsbV, RsbW, and RsbY in regulating σ B activity in Bacillus cereus . J Bacteriol 187:5846–5851
     [Google Scholar]
  47. Vijay K., Brody M. S., Fredlund E., Price C. W. 2000; A PP2C phosphatase containing a PAS domain is required to convey signals of energy stress to the σ B transcription factor of Bacillus subtilis . Mol Microbiol 35:180–188
     [Google Scholar]
  48. Viollier P. H., Kelemen G. H., Dale G. E., Nguyen K. T., Buttner M. J., Thompson C. J. 2003; Specialized osmotic stress response systems involve multiple SigB-like sigma factors in Streptomyces coelicolor . Mol Microbiol 47:699–714
     [Google Scholar]
  49. Voelker U., Voelker A., Maul B., Hecker M., Dufour A., Haldenwang W. G. 1995; Separate mechanisms activate σ B of Bacillus subtilis in response to environmental and metabolic stresses. J Bacteriol 177:3771–3780
     [Google Scholar]
  50. Zimmer M. A., Tiu J., Collins M. A., Ordal G. W. 2000; Selective methylation changes on the Bacillus subtilis chemotaxis receptor McpB promote adaptation. J Biol Chem 275:24264–24272
     [Google Scholar]
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Novel σB regulation modules of Gram-positive bacteria involve the use of complex hybrid histidine kinases
Microbiology 157, 3 (2011); https://doi.org/10.1099/mic.0.045740-0
/content/journal/micro/10.1099/mic.0.045740-0
/content/journal/micro/10.1099/mic.0.045740-0
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