The starvation-stress response of serovar Typhimurium requires σ-, but not CpxR-regulated extracytoplasmic functions Free

Abstract

Starvation of serovar Typhimurium ( Typhimurium) for an exogenous source of carbon and energy (C-starvation) induces the starvation-stress response (SSR). The SSR functions to (i) maintain viability during long-term C-starvation and (ii) generate cross-resistance to other environmental stresses. The SSR is, at least partially, under the control of the alternative sigma factor, σ. It is hypothesized that C-starvation causes cell envelope stresses that could induce the σ and/or Cpx regulons, both of which control extracytoplasmic functions and, thus, may play a role in the regulation of the SSR. In support of this hypothesis, Western blot analysis showed that the relative levels of σ increased during C-starvation, peaking after approximately 72 h of C-starvation; in contrast, CpxR levels remained relatively constant from exponential phase up to 72 h of C-starvation. To determine if σ, and thus the regulon it controls, is an essential component of the SSR, several mutant strains were compared for their abilities to survive long-term C-starvation and to develop C-starvation-induced (CSI) cross-resistances. An mutant strain was significantly impaired in both long-term C-starvation survival (LT-CSS) and in CSI cross-resistance to challenges with 20 mM HO for 40 min, 55 °C for 16 min, pH 31 for 60 min and 8702 USP U polymyxin B ml (PmB) for 60 min, to varying degrees. These results suggest that C-starvation can generate signals that induce the regulon and that one or more members of the σ regulon are required for maximal SSR function. Furthermore, evidence suggests that the σ and σ regulons function through separate mechanisms in the SSR. In contrast, C-starvation does not appear to generate signals required for Cpx regulon induction which support the findings that it is not required for LT-CSS or cross-resistance to HO, pH 31 or PmB challenges. However, it was required to achieve maximal cross-resistance to 55 °C. Therefore, σ is a key regulatory component of the SSR and represents an additional σ factor required for the SSR of .

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-1-113
2002-01-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/1/1480113a.html?itemId=/content/journal/micro/10.1099/00221287-148-1-113&mimeType=html&fmt=ahah

References

  1. Ades S. E., Connolly L. E., Alba B. M., Gross C. A. 1999; The Escherichia coli σE-dependent extracytoplasmic stress response is controlled by the regulated proteolysis of an anti-σ factor. Genes Dev 13:2449–2461 [CrossRef]
    [Google Scholar]
  2. Betton J. M., Sassoon N., Hofnung M., Laurent M. 1998; Degradation versus aggregation of misfolded maltose-binding protein in the periplasm of Escherichia coli . J Biol Chem 273:8897–8902 [CrossRef]
    [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 Biochem 72:248–254 [CrossRef]
    [Google Scholar]
  4. Chan R. K., Botstein D., Watanabe T., Ogata Y. 1972; Specialized transduction of tetracycline resistance by phage P22 in Salmonella typhimurium . II. Properties of a high-frequency-transducing lysate. Virology 50:883–898 [CrossRef]
    [Google Scholar]
  5. Connolly L., De Las Penas A., Alba B. M., Gross C. A. 1997; The response to extracytoplasmic stress in Escherichia coli is controlled by partially overlapping pathways. Genes Dev 11:2012–2021 [CrossRef]
    [Google Scholar]
  6. Danese P. N., Silhavy T. J. 1997; The σE and the Cpx signal transduction systems control the synthesis of periplasmic protein-folding enzymes in Escherichia coli . Genes Dev 11:1183–1193 [CrossRef]
    [Google Scholar]
  7. Danese P. N., Silhavy T. J. 1998; CpxP, a stress-combative member of the Cpx regulon. J Bacteriol 180:831–839
    [Google Scholar]
  8. Danese P. N., Snyder W. B., Cosma C. L., Davis L. J. B., Silhavy T. J. 1995; The Cpx two-component signal transduction pathway of Escherichia coli regulates transcription of the gene specifying the stress-inducible periplasmic protease, DegP. Genes Dev 9:387–398 [CrossRef]
    [Google Scholar]
  9. Dartigalongue C., Missiakas D., Raina S. 2001; Characterization of the Escherichia coli σE regulon. J Biol Chem 276:20866–20875 [CrossRef]
    [Google Scholar]
  10. De Las Penas A., Connolly L., Gross C. A. 1997a; σE is an essential sigma factor in Escherichia coli . J Bacteriol 179:6862–6864
    [Google Scholar]
  11. De Las Penas A., Connolly L., Gross C. A. 1997b; The σE-mediated response to extracytoplasmic stress in Escherichia coli is transduced by RseA and RseB, two negative regulators of σE. Mol Microbiol 24:373–385 [CrossRef]
    [Google Scholar]
  12. Daugelavicius R., Bakiene E., Bamford D. H. 2000; Stages of polymyxin B interaction with the Escherichia coli cell envelope. Antimicrob Agents Chemother 44:2969–2978 [CrossRef]
    [Google Scholar]
  13. Erickson J. W., Gross C. A. 1989; Identification of the σE subunit of Escherichia coli RNA polymerase, a second alternative σ factor involved in high-temperature gene expression. Genes Dev 3:1462–1471 [CrossRef]
    [Google Scholar]
  14. Fang F. C., Libby S. J., Buchmeier N. A., Loewen P. C., Switala J., Harwood J., Guiney D. G. 1992; The alternative σ factor KatF (RpoS) regulates Salmonella virulence. Proc Natl Acad Sci USA 89:11978–11982 [CrossRef]
    [Google Scholar]
  15. Foster J. W., Spector M. P. 1995; How Salmonella survive against the odds. Annu Rev Microbiol 49:145–174 [CrossRef]
    [Google Scholar]
  16. Hengge-Aronis R. others 1996; Regulation of gene expression during entry into stationary phase. In Escherichia coli and Salmonella, Cellular and Molecular Biology , 2nd edn. pp 1497–1512 Edited by Neidhardt F. C. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  17. Hiratsu K., Amemura M., Nashimoto H., Shinagawa H., Makino K. 1995; The rpoE gene of Escherichia coli , which encodes σE, is essential for bacterial growth at high temperature. J Bacteriol 177:2918–2922
    [Google Scholar]
  18. Hoseith S. K., Stocker B. A. D. 1981; Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 291:238–239 [CrossRef]
    [Google Scholar]
  19. Humphreys S., Stevenson A., Bacon A., Weinhardt A. B., Roberts M. 1999; The alternative sigma factor, σE, is critically important for the virulence of Salmonella typhimurium . Infect Immun 67:1560–1568
    [Google Scholar]
  20. Ibanez-Ruiz M., Robbe-Saule V., Hermant D., Labrude V., Norel F. 2000; Identification of RpoS (σS)-regulated genes in Salmonella enterica serovar Typhimurium. J Bacteriol 182:5749–5756 [CrossRef]
    [Google Scholar]
  21. Jenkins D. E., Schultz J. E., Matin A. 1988; Starvation-induced cross-protection against heat or H2O2 challenge in Escherichia coli . J Bacteriol 170:3910–3914
    [Google Scholar]
  22. Jenkins D. E., Auger E. A., Matin A. 1991; Role of RpoH, a heat shock regulator protein, in Escherichia coli carbon starvation protein synthesis and survival. J Bacteriol 173:1992–1996
    [Google Scholar]
  23. Lange R., Hengge-Aronis R. 1991; Identification of a central regulator of stationary-phase gene expression in Escherichia coli . Mol Microbiol 5:49–59 [CrossRef]
    [Google Scholar]
  24. 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]
    [Google Scholar]
  25. McCann M. P., Kidwell J. P., Matin A. 1991; The putative σ factor KatF has a central role in development of starvation-mediated general resistance in Escherichia coli . J Bacteriol 173:4188–4194
    [Google Scholar]
  26. McLeod G. I., Spector M. P. 1996; Starvation- and stationary-phase-induced resistance to the antimicrobial peptide polymyxin B in Salmonella typhimurium is RpoS (σS) independent and occurs through both phoP -dependent and -independent pathways. J Bacteriol 178:3683–3688
    [Google Scholar]
  27. Maloy S. R. 1990 Experimental Techniques in Bacterial Genetics Boston, MA: Jones & Bartlett;
    [Google Scholar]
  28. Mecsas J., Rouviere P. E., Erickson J. W., Donohue T. J., Gross C. A. 1993; The activity of σE, an Escherichia coli heat-inducible σ-factor, is modulated by expression of outer membrane proteins. Genes Dev 7:2618–2628 [CrossRef]
    [Google Scholar]
  29. Miller J. H. 1972 Experiments in Molecular Genetics Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  30. Missiakas D., Raina S. 1997a; Protein misfolding in the cell envelope of Escherichia coli , new signaling pathways. Trends Biochem Sci 22:59–63 [CrossRef]
    [Google Scholar]
  31. Missiakas D., Raina S. 1997b; Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli , role of two new phosphoprotein phosphatases PrpA and PrpB. EMBO J 16:1670–1685 [CrossRef]
    [Google Scholar]
  32. Missiakas D., Raina S. 1998; The extracytoplasmic function sigma factors, role and regulation. Mol Microbiol 28:1059–1066 [CrossRef]
    [Google Scholar]
  33. Missiakas D., Mayer M. P., Lemaire M., Georgopoulos C., Raina S. 1997; Modulation of the Escherichia coli σE (RpoE) heat-shock transcription-factor activity by the RseA, RseB, and RseC proteins. Mol Microbiol 24:355–371 [CrossRef]
    [Google Scholar]
  34. Muffler A., Barth M., Marschall C., Hengge-Aronis R. 1997; Heat shock regulation of σS turnover, a role for DnaK and relationship between stress responses mediated by σS and σ32 in Escherichia coli . J Bacteriol 179:445–452
    [Google Scholar]
  35. Neidhardt F. C., Bloch P. L., Smith D. F. 1974; Culture medium for enterobacteria. J Bacteriol 119:736–747
    [Google Scholar]
  36. Nitta T., Nagamitsu H., Murata M., Izu H., Yamada M. 2000; Function of the σE regulon in dead-cell lysis in stationary-phase Escherichia coli . J Bacteriol 182:5231–5237 [CrossRef]
    [Google Scholar]
  37. O’Neal C. R., Gabriel W. M., Turk A. K., Libby S. J., Fang F. C., Spector M. P. 1994; RpoS is necessary for both positive and negative regulation of starvation-survival genes during phosphate, carbon, and nitrogen starvation in Salmonella typhimurium . J Bacteriol 176:4610–4616
    [Google Scholar]
  38. Pallen M. J., Wren B. W. 1997; The HtrA family of serine proteases. Mol Microbiol 26:209–221 [CrossRef]
    [Google Scholar]
  39. Pogliano J., Lynch A. S., Belin D., Lin E. C. C., Beckwith J. 1997; Regulation of Escherichia coli cell envelope proteins involved in protein folding and degradation by the Cpx two-component system. Genes Dev 11:1169–1182 [CrossRef]
    [Google Scholar]
  40. Raina S., Missiakas K., Georgopoulos C. 1995; The rpoE gene encoding the σE24) heat shock sigma factor of Escherichia coli . EMBO J 14:1043–1055
    [Google Scholar]
  41. Raivio T. L., Silhavy T. J. 1999; The σE and Cpx regulatory pathways, overlapping but distinct envelope stress responses. Curr Opin Microbiol 2:159–165 [CrossRef]
    [Google Scholar]
  42. Rouviere P. E., De Las Penas A., Mecsas J., Lu C. Z., Rudd K. E., Gross C. A. 1995; rpoE , the gene encoding the second heat-shock sigma factor, σE, in Escherichia coli . EMBO J 14:1032–1042
    [Google Scholar]
  43. Seymour R. L., Mishra P. V., Khan M. A., Spector M. P. 1996; Essential roles of core starvation-stress response loci in carbon-starvation-inducible cross-resistance and hydrogen peroxide-inducible adaptive resistance to oxidative challenge in Salmonella typhimurium . Mol Microbiol 20:497–505 [CrossRef]
    [Google Scholar]
  44. Skorko-Glonek J., Zurawa D., Kuczwara E., Wozniak M., Wypych Z., Lipinska B. 1999; The Escherichia coli heat shock protease HtrA participates in defense against oxidative stress. Mol Gen Genet 262:342–350 [CrossRef]
    [Google Scholar]
  45. Spector M. P. 1998; The starvation-stress response (SSR) of Salmonella . Adv Microb Physiol 40:233–279
    [Google Scholar]
  46. Spector M. P., Cubitt C. L. 1992; Starvation-inducible loci of Salmonella typhimurium , regulation and roles in starvation survival. Mol Microbiol 6:1467–1476 [CrossRef]
    [Google Scholar]
  47. Spector M. P., Garcia del Portillo F., Bearson S. M., Mahmud A., Magut M., Finlay B. B., Dougan G., Foster J. W., Pallen M. J. 1999; The rpoS -dependent starvation-stress response locus stiA encodes a nitrate reductase ( narZYWV ) required for carbon-starvation-inducible thermotolerance and acid tolerance in Salmonella typhimurium . Microbiology 145:3035–3045
    [Google Scholar]
  48. Spiess C., Beil A., Ehrmann M. 1999; A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347 [CrossRef]
    [Google Scholar]
  49. Wang R. F., Kushner S. R. 1991; Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli . Gene 100:195–199 [CrossRef]
    [Google Scholar]
  50. Yura T., Nakahigashi K. 1999; Regulation of the heat-shock response. Curr Opin Microbiol 2:153–158 [CrossRef]
    [Google Scholar]
  51. Yura T., Nakahigashi K., Kanemori M. 1996; Transcriptional regulation of stress-inducible genes in procaryotes. In Experientia Supplementum, Stress-Inducible Cellular Responses pp 165–181 Edited by Feige U.and others Basel: Birkhauser;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-1-113
Loading
/content/journal/micro/10.1099/00221287-148-1-113
Loading

Data & Media loading...

Most cited Most Cited RSS feed