1887

Abstract

The stationary-phase response mediated by the RpoS sigma factor (σ, σ) has been widely studied as a general mechanism of activation of highly diverse genes that maintain cell viability. In bacteria, genes for diverse functions have been associated with this response, showing that bacteria use a large number of functions to contend with adverse conditions in their environment. However, little is known about how the genes have been functionally recruited in diverse organisms. In this work, we address the analysis of genes regulated by σ, based on a comparative genomic-scale analysis considering four versatile bacterial species that represent different lifestyles and taxonomic groups, K-12, and , as well as the extent of conservation in bacterial genomes, as a means of assessing the evolution of this sigmulon across all organisms completely sequenced. The analysis presented here shows that genes associated with the σ response have been recruited from diverse regulons to achieve a global response. In addition, and based on the distribution of orthologues, we show a group of genes that is highly conserved among all organisms, mainly associated with glycerol metabolism, as well as diverse functional genes recruited in a lineage-specific manner.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.042937-0
2011-05-01
2019-10-14
Loading full text...

Full text loading...

/deliver/fulltext/micro/157/5/1393.html?itemId=/content/journal/micro/10.1099/mic.0.042937-0&mimeType=html&fmt=ahah

References

  1. Benson D. A. , Karsch-Mizrachi I. , Lipman D. J. , Ostell J. , Wheeler D. L. . ( 2008; ). GenBank. . Nucleic Acids Res 36: Database issue D25–D30. [CrossRef] [PubMed]
    [Google Scholar]
  2. Brisson D. , Vohl M. C. , St-Pierre J. , Hudson T. J. , Gaudet D. . ( 2001; ). Glycerol: a neglected variable in metabolic processes?. Bioessays 23:, 534–542. [CrossRef] [PubMed]
    [Google Scholar]
  3. Caimano M. J. , Eggers C. H. , Hazlett K. R. , Radolf J. D. . ( 2004; ). RpoS is not central to the general stress response in Borrelia burgdorferi but does control expression of one or more essential virulence determinants. . Infect Immun 72:, 6433–6445. [CrossRef] [PubMed]
    [Google Scholar]
  4. Chen G. , Patten C. L. , Schellhorn H. E. . ( 2004; ). Positive selection for loss of RpoS function in Escherichia coli . . Mutat Res 554:, 193–203.[PubMed] [CrossRef]
    [Google Scholar]
  5. Chiang S. M. , Schellhorn H. E. . ( 2010; ). Evolution of the RpoS regulon: origin of RpoS and the conservation of RpoS-dependent regulation in bacteria. . J Mol Evol 70:, 557–571. [CrossRef] [PubMed]
    [Google Scholar]
  6. Dong T. , Chiang S. M. , Joyce C. , Yu R. , Schellhorn H. E. . ( 2009; ). Polymorphism and selection of rpoS in pathogenic Escherichia coli . . BMC Microbiol 9:, 118. [CrossRef] [PubMed]
    [Google Scholar]
  7. Dufour Y. S. , Kiley P. J. , Donohue T. J. . ( 2010; ). Reconstruction of the core and extended regulons of global transcription factors. . PLoS Genet 6:, e1001027. [CrossRef] [PubMed]
    [Google Scholar]
  8. Finn R. D. , Mistry J. , Tate J. , Coggill P. , Heger A. , Pollington J. E. , Gavin O. L. , Gunasekaran P. , Ceric G. et al. ( 2010; ). The Pfam protein families database. . Nucleic Acids Res 38: Database issue D211–D222. [CrossRef] [PubMed]
    [Google Scholar]
  9. Fitch W. M. . ( 1970; ). Distinguishing homologous from analogous proteins. . Syst Zool 19:, 99–113. [CrossRef] [PubMed]
    [Google Scholar]
  10. Gama-Castro S. , Jiménez-Jacinto V. , Peralta-Gil M. , Santos-Zavaleta A. , Peñaloza-Spinola M. I. , Contreras-Moreira B. , Segura-Salazar J. , Muñiz-Rascado L. , Martínez-Flores I. et al. ( 2008; ). RegulonDB (version 6.0): gene regulation model of Escherichia coli K-12 beyond transcription, active (experimental) annotated promoters and Textpresso navigation. . Nucleic Acids Res 36: Database issue D120–D124. [CrossRef] [PubMed]
    [Google Scholar]
  11. Hales L. M. , Shuman H. A. . ( 1999; ). The Legionella pneumophila rpoS gene is required for growth within Acanthamoeba castellanii . . J Bacteriol 181:, 4879–4889.[PubMed]
    [Google Scholar]
  12. Hecker M. , Pané-Farré J. , Völker U. . ( 2007; ). SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria. . Annu Rev Microbiol 61:, 215–236. [CrossRef] [PubMed]
    [Google Scholar]
  13. Hengge-Aronis R. . ( 1996; ). Back to log phase: σS as a global regulator in the osmotic control of gene expression in Escherichia coli . . Mol Microbiol 21:, 887–893. [CrossRef] [PubMed]
    [Google Scholar]
  14. Hengge-Aronis R. . ( 1999; ). Interplay of global regulators and cell physiology in the general stress response of Escherichia coli . . Curr Opin Microbiol 2:, 148–152. [CrossRef] [PubMed]
    [Google Scholar]
  15. Hengge-Aronis R. . ( 2000; ). A role for the σS subunit of RNA polymerase in the regulation of bacterial virulence. . Adv Exp Med Biol 485:, 85–93. [CrossRef] [PubMed]
    [Google Scholar]
  16. Hengge-Aronis R. . ( 2002; ). Signal transduction and regulatory mechanisms involved in control of the σS (RpoS) subunit of RNA polymerase. . Microbiol Mol Biol Rev 66:, 373–395. [CrossRef] [PubMed]
    [Google Scholar]
  17. Janga S. C. , Moreno-Hagelsieb G. . ( 2004; ). Conservation of adjacency as evidence of paralogous operons. . Nucleic Acids Res 32:, 5392–5397. [CrossRef] [PubMed]
    [Google Scholar]
  18. Kehry M. R. , Dahlquist F. W. . ( 1982; ). The methyl-accepting chemotaxis proteins of Escherichia coli. Identification of the multiple methylation sites on methyl-accepting chemotaxis protein I. . J Biol Chem 257:, 10378–10386.[PubMed]
    [Google Scholar]
  19. King T. , Seeto S. , Ferenci T. . ( 2006; ). Genotype-by-environment interactions influencing the emergence of rpoS mutations in Escherichia coli populations. . Genetics 172:, 2071–2079. [CrossRef] [PubMed]
    [Google Scholar]
  20. Liu R. , Ochman H. . ( 2007; ). Stepwise formation of the bacterial flagellar system. . Proc Natl Acad Sci U S A 104:, 7116–7121. [CrossRef] [PubMed]
    [Google Scholar]
  21. Loewen P. C. , Hu B. , Strutinsky J. , Sparling R. . ( 1998; ). Regulation in the rpoS regulon of Escherichia coli . . Can J Microbiol 44:, 707–717. [CrossRef] [PubMed]
    [Google Scholar]
  22. Lozada-Chávez I. , Janga S. C. , Collado-Vides J. . ( 2006; ). Bacterial regulatory networks are extremely flexible in evolution. . Nucleic Acids Res 34:, 3434–3445. [CrossRef] [PubMed]
    [Google Scholar]
  23. Martínez-García E. , Tormo A. , Navarro-Llorens J. M. . ( 2001; ). Further studies on RpoS in enterobacteria: identification of rpoS in Enterobacter cloacae and Kluyvera cryocrescens . . Arch Microbiol 175:, 395–404. [CrossRef] [PubMed]
    [Google Scholar]
  24. Masuda N. , Church G. M. . ( 2003; ). Regulatory network of acid resistance genes in Escherichia coli . . Mol Microbiol 48:, 699–712. [CrossRef] [PubMed]
    [Google Scholar]
  25. Monsieurs P. , De Keersmaecker S. , Navarre W. W. , Bader M. W. , De Smet F. , McClelland M. , Fang F. C. , De Moor B. , Vanderleyden J. , Marchal K. . ( 2005; ). Comparison of the PhoPQ regulon in Escherichia coli and Salmonella typhimurium . . J Mol Evol 60:, 462–474. [CrossRef] [PubMed]
    [Google Scholar]
  26. Núñez C. , Esteve-Núñez A. , Giometti C. , Tollaksen S. , Khare T. , Lin W. , Lovley D. R. , Methé B. A. . ( 2006; ). DNA microarray and proteomic analyses of the RpoS regulon in Geobacter sulfurreducens . . J Bacteriol 188:, 2792–2800. [CrossRef] [PubMed]
    [Google Scholar]
  27. Paget M. S. , Helmann J. D. . ( 2003; ). The σ70 family of sigma factors. . Genome Biol 4:, 203. [CrossRef] [PubMed]
    [Google Scholar]
  28. Sierro N. , Makita Y. , de Hoon M. , Nakai K. . ( 2008; ). DBTBS: a database of transcriptional regulation in Bacillus subtilis containing upstream intergenic conservation information. . Nucleic Acids Res 36: Database issue D93–D96. [CrossRef] [PubMed]
    [Google Scholar]
  29. Tatusov R. L. , Koonin E. V. , Lipman D. J. . ( 1997; ). A genomic perspective on protein families. . Science 278:, 631–637. [CrossRef] [PubMed]
    [Google Scholar]
  30. Tramonti A. , De Canio M. , Bossa F. , De Biase D. . ( 2003; ). Stability and oligomerization of recombinant GadX, a transcriptional activator of the Escherichia coli glutamate decarboxylase system. . Biochim Biophys Acta 1647:, 376–380.[PubMed] [CrossRef]
    [Google Scholar]
  31. Völker U. , Maul B. , Hecker M. . ( 1999; ). Expression of the σB-dependent general stress regulon confers multiple stress resistance in Bacillus subtilis . . J Bacteriol 181:, 3942–3948.[PubMed]
    [Google Scholar]
  32. Weber H. , Polen T. , Heuveling J. , Wendisch V. F. , Hengge R. . ( 2005; ). Genome-wide analysis of the general stress response network in Escherichia coli: σS-dependent genes, promoters, and sigma factor selectivity. . J Bacteriol 187:, 1591–1603. [CrossRef] [PubMed]
    [Google Scholar]
  33. Weitzman P. D. . ( 1981; ). Unity and diversity in some bacterial citric acid-cycle enzymes. . Adv Microb Physiol 22:, 185–244. [CrossRef] [PubMed]
    [Google Scholar]
  34. Woodsmall R. M. , Benson D. A. . ( 1993; ). Information resources at the National Center for Biotechnology Information. . Bull Med Libr Assoc 81:, 282–284.[PubMed]
    [Google Scholar]
  35. Zambrano M. M. , Siegele D. A. , Almirón M. , Tormo A. , Kolter R. . ( 1993; ). Microbial competition: Escherichia coli mutants that take over stationary phase cultures. . Science 259:, 1757–1760. [CrossRef] [PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.042937-0
Loading
/content/journal/micro/10.1099/mic.0.042937-0
Loading

Data & Media loading...

[PDF](7 KB)

PDF

A single linkage-clustering algorithm with none leaf order optimization was applied with Manhattan distance as similarity measure [PDF](547 KB)

PDF
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