Invasiveness in chickens, stress resistance and RpoS status of wild-type subsp. serovar Typhimurium definitive type 104 and serovar Enteritidis phage type 4 strains Free

Abstract

The heat and acid resistance and the ability to survive airdrying on commonly used kitchen surfaces were assessed for clinical and environmental strains of subsp. serovar Typhimurium, definitive type (DT) 104. Three out of thirty-eight strains of DT 104 were found to be more sensitive in stationary phase to the stresses examined than the other strains. This compares to a previous study by the authors which showed that seven out of forty serovar Enteritidis phage type (PT) 4 strains were more sensitive. RpoS activity was examined indirectly in selected strains of DT 104 and PT 4. In those with normal stress resistance a 100-fold induction of an RpoS-dependent /′:: fusion was observed upon entry into stationary phase. The sensitive strains examined showed either no induction or a reduced level of /′:: expression. The gene was sequenced from these strains and three were found to harbour mutations including one deletion, one base-pair substitution resulting in a nonsense codon, and one insertion causing a frameshift resulting in an early stop codon. Strains with negligible or reduced /′:: expression had low stress resistance. All strains of DT 104 could be recovered from liver and spleen tissues of infected hens 14 d post-infection, but one with no induction of /′:: expression was significantly less likely to be recovered from chicken reproductive tissues, liver or spleen than the majority of other strains, including one with reduced /′:: expression. This work has demonstrated that clinical and environmental strains of DT 104 and PT 4 not infrequently harbour mutations in the allele. It is possible that the mutations may have occurred during the initial isolation of the strains. The ability of a strain to cause infection, however, also depends on factors such as host susceptibility and dose.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-146-12-3227
2000-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/146/12/1463227a.html?itemId=/content/journal/micro/10.1099/00221287-146-12-3227&mimeType=html&fmt=ahah

References

  1. Allen-Vercoe E., Collighan R., Woodward M. J. 1998; The variant rpoS allele of S. enteritidis strain 27655R does not affect virulence in a chick model nor constitutive curliation but does generate a cold-sensitive phenotype. FEMS Microbiol Lett 167:245–253 [CrossRef]
    [Google Scholar]
  2. Altekruse S. F., Cohen M. L., Swerdlow D. L. 1997; Emerging foodborne diseases. Emerg Infect Dis 3:285–293 [CrossRef]
    [Google Scholar]
  3. Anonymous 1997; Multidrug resistant Salmonella typhimurium. Fact sheet no. 139, Division of Emerging and Other Communicable Diseases Surveillance and Control. Geneva, Switzerland: World Health Organization;
    [Google Scholar]
  4. Anonymous 1999; Salmonella infections, England and Wales: reports to the PHLS (Salmonella data set). Commun Dis Rep Rev 9:10
    [Google Scholar]
  5. Bearson S. M. D., Benjamin W. H. Jr, Swords W. E., Foster J. W. 1996; Acid shock induction of RpoS is mediated by the mouse virulence gene mviA of Salmonella typhimurium. J Bacteriol 178:2572–2579
    [Google Scholar]
  6. Cox J. M. 1995; Salmonella enteritidis: virulence factors and invasive infection in poultry. Trends Food Sci Technol 6:407–410 [CrossRef]
    [Google Scholar]
  7. Coyle E. F., Ribeiro C. D., Howard A. J., Palmer S. R., Jones H. I., Ward L., Rowe B. 1988; The Salmonella enteritidis phage type 4 infection associated with hen eggs. Lancet ii:1295–1296
    [Google Scholar]
  8. 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]
  9. Fang F. C., Chen C. Y., Guiney D. G., Xu Y. 1996; Identification of σS-regulated genes in Salmonella typhimurium: complementary regulatory interactions between σS and cyclic AMP receptor protein. J Bacteriol 178:5112–5120
    [Google Scholar]
  10. Guiney D. G., Libby S., Fang F. C., Krause M., Fierer J. 1995; Growth-phase regulation of plasmid virulence genes in Salmonella. Trends Microbiol 3:275–279 [CrossRef]
    [Google Scholar]
  11. Gulig P. A., Danbara H., Guiney D. G., Lax A. J., Norel F., Rhen M. 1993; Molecular analysis of spv virulence genes of the salmonella virulence plasmids. Mol Microbiol 10:825–830
    [Google Scholar]
  12. Halavatkar H., Barrow P. L. 1993; The role of a 54-kb plasmid in the virulence of strains of Salmonella enteritidis of phage type 4 for chicken and mice. J Med Microbiol 38:171–176 [CrossRef]
    [Google Scholar]
  13. Hill P. J., Rees C. E. D., Winson M. K., Stewart G. S. A. B. 1993; The application of lux genes. Biotechnol Appl Biochem 17:3–14
    [Google Scholar]
  14. Humphrey T. J., Slater E., McAlpine K., Rowbury R. J., Gilbert R. J. 1995; Salmonella enteritidis phage type 4 isolates more tolerant of heat, acid, or hydrogen peroxide also survive longer on surfaces. Appl Environ Microbiol 61:3161–3164
    [Google Scholar]
  15. Humphrey T. J., Williams A., McAlpine K., Lever M. S., Guard-Petter J., Cox J. M. 1996; Isolates of Salmonella enterica Enteritidis PT 4 with enhanced heat and acid tolerance are more virulent in mice and more invasive in chicken. Epidemiol Infect 117:79–88 [CrossRef]
    [Google Scholar]
  16. Humphrey T. J., Williams A., McAlpine K., Jørgensen F., O’Byrne C. 1998; Pathogenicity in isolates of Salmonella enterica serotype Enteritidis PT 4 which differ in RpoS expression: effects of growth phase and low temperature. Epidemiol Infect 121:295–301 [CrossRef]
    [Google Scholar]
  17. 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]
  18. Ivanova A., Renshaw M., Guntaka R. V., Eisenstark A. 1992; DNA base sequence variability in katF (putative sigma factor) gene of Escherichia coli. Nucleic Acid Res 20:5479–5480 [CrossRef]
    [Google Scholar]
  19. Lange R., Hengge-Aronis R. 1994; The cellular concentration of the σS subunit of RNA polymerase in Escherichia coli is controlled at the levels of transcription, translation, and protein stability. Genes Dev 8:1600–1612 [CrossRef]
    [Google Scholar]
  20. Leach S. A., Williams A., Davies A. C., Wilson J., Marsh P. D., Humphrey T. J. 1999; Aerosol route of experimental infection enhances the contamination of intact eggs and muscle of experimentally laying hens by Salmonella typhimurium DT 104. FEMS Microbiol Lett 171:203–207 [CrossRef]
    [Google Scholar]
  21. Loewen P. C., Hengge-Aronis R. 1994; The role of the sigma factor σs (KatF) in bacterial global regulation. . Annu Rev Microbiol 48:53–80 [CrossRef]
    [Google Scholar]
  22. Mahan M. J., Slauch J. M., Mekalanos J. J. 1996; Environmental regulation of virulence gene expression in Escherichia, Salmonella and Shigella spp. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp. 2803–2815Edited by Neidhardt F. C.others Washington, DC: American Society for Microbiology;
    [Google Scholar]
  23. Nickerson C. A., Curtiss R. III 1997; Role of sigma factor RpoS in initial stages of Salmonella typhimurium infection. . Infect Immun 65:1814–1823
    [Google Scholar]
  24. Picard B., Garcia J. S., Gouriou S., Duriez P., Brahimi N., Bingen E., Elion J., Denamur E. 1999; The link between phylogeny and virulence in Escherichia coli extraintestinal infection. Infect Immun 67:546–553
    [Google Scholar]
  25. Potts M. 1994; Desiccation tolerance of prokaryotes. . Microbiol Rev 58:755–805
    [Google Scholar]
  26. Pratt L. A., Silhavy T. J. 1996; The response regulator SprE controls the stability of RpoS. Proc Natl Acad Sci USA 93:2488–2492 [CrossRef]
    [Google Scholar]
  27. Rajashekara G., Munir S., Alexeyev M. F., Halvorson D. A., Wells C. L., Nagaraja K. V. 2000; Pathogenic role of SEF14, SEF17, and SEF21 fimbriae in Salmonella enterica serovar Enteritidis infection of chickens. Appl Environ Microbiol 66:1759–1763 [CrossRef]
    [Google Scholar]
  28. Rampling A., Anderson J. R., Upson R., Peters E., Ward L. R., Rowe B. 1989; Salmonella enteritidis phage type 4 infection of broiler chickens: a hazard to public health. Lancet ii:436–438
    [Google Scholar]
  29. Schweder T., Lee K.-H., Lomovskaya O., Matin A. 1996; Regulation of Escherichia coli starvation sigma factor σS by ClpXP protease. . J Bacteriol 178:470–476
    [Google Scholar]
  30. Swift S., Stewart G. S. A. B. 1994; Luminescence as a signal of spvA expression. In Bioluminescence and Chemiluminescence. Fundamentals and Applied Aspects pp. 93–96Edited by Campbell A. K. , Kricka L. J., Stanley P. E. Chichester: Wiley;
    [Google Scholar]
  31. Swift S., Winson M. K., Chan P. F.11 other authors 1993; A novel strategy for the isolation of luxI homologues: evidence for the widespread distribution of a LuxR:LuxI superfamily in enteric bacteria. Mol Microbiol 10:511–520 [CrossRef]
    [Google Scholar]
  32. Threlfall E. J., Hampton M. D., Schofield S. L., Ward L. R., Frost J. A., Rowe B. 1996; Epidemiological application of differentiating multiresistant Salmonella typhimurium DT 104 by plasmid profile. Commun Dis Rep Rev 6:R155–R159
    [Google Scholar]
  33. Visick J. E., Clarke S. 1997; RpoS- and OxyR-independent induction of HPI catalase at stationary phase in Escherichia coli and identification of rpoS mutations in common laboratory strains. . J Bacteriol 179:4158–4163
    [Google Scholar]
  34. Wall P. G., Morgan D., Lamden K., Ryan M., Griffin M., Threlfall E. J., Ward L. R., Rowe B. 1994; A case control study of infection with an epidemic strain of multi-resistant Salmonella typhimurium DT 104 in England and Wales. . Commun Dis Rep Rev 4:R130–R140
    [Google Scholar]
  35. Waterman S. R., Small P. L. C. 1996; Characterization of the acid resistance phenotype and rpoS alleles of shiga-like toxin-producing Escherichia coli. Infect Immun 64:2808–2811
    [Google Scholar]
  36. Williams A., Davies A. C., Wilson J., Marsh P. D., Leach S., Humphrey T. J. 1998; Contamination of the contents of intact eggs by Salmonella typhimurium DT 104. Vet Rec 143:562–563 [CrossRef]
    [Google Scholar]
  37. Wilmes-Riesenberger M. R., Foster J. W., Curtiss R. III 1997; An altered rpoS allele contributes to the avirulence of Salmonella typhimurium LT2. Infect Immun 65:203–210
    [Google Scholar]
  38. 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]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-146-12-3227
Loading
/content/journal/micro/10.1099/00221287-146-12-3227
Loading

Data & Media loading...

Most cited Most Cited RSS feed