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. 1995 Jul;63(7):2755–2761. doi: 10.1128/iai.63.7.2755-2761.1995

The Salmonella dublin virulence plasmid mediates systemic but not enteric phases of salmonellosis in cattle.

T S Wallis 1, S M Paulin 1, J S Plested 1, P R Watson 1, P W Jones 1
PMCID: PMC173368  PMID: 7790094

Abstract

Plasmid-bearing and plasmid-free isolates and a plasmid-cured strain of Salmonella dublin were compared for virulence in calves. The plasmid-bearing strains were highly virulent, causing severe enteric and systemic disease with high mortality. In contrast, the plasmid-free strains caused diarrhea but only low mortality. The infection kinetics of a wild-type and a derivative plasmid-cured strain were compared. Both strains were isolated in high numbers from intestinal sites at 3 and 6 days after oral challenge and were isolated at comparable frequencies from systemic sites at 3 days, but not at 6 days, when the wild-type strain was predominant. The strains were equally invasive in intestinal epithelia with and without Peyer's patch and elicited comparable secretory and inflammatory responses and intestinal pathology in ligated ileal loops. The effect of the virulence plasmid on growth kinetics and on the outer membrane protein profile was assessed in an in vivo growth chamber. The virulence plasmid did not influence either extracellular growth or the expression of major outer membrane proteins. These observations demonstrate that the virulence plasmid is not involved in either the enteric phase of infection or the systemic dissemination of S. dublin but probably mediates the persistence of S. dublin at systemic sites.

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Selected References

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  1. Achtman M., Mercer A., Kusecek B., Pohl A., Heuzenroeder M., Aaronson W., Sutton A., Silver R. P. Six widespread bacterial clones among Escherichia coli K1 isolates. Infect Immun. 1983 Jan;39(1):315–335. doi: 10.1128/iai.39.1.315-335.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Barrow P. A., Simpson J. M., Lovell M. A., Binns M. M. Contribution of Salmonella gallinarum large plasmid toward virulence in fowl typhoid. Infect Immun. 1987 Feb;55(2):388–392. doi: 10.1128/iai.55.2.388-392.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Carlson G. P., Kaneko J. J. Isolation of leukocytes from bovine peripheral blood. Proc Soc Exp Biol Med. 1973 Mar;142(3):853–856. doi: 10.3181/00379727-142-37131. [DOI] [PubMed] [Google Scholar]
  4. Chopra A. K., Houston C. W., Peterson J. W., Prasad R., Mekalanos J. J. Cloning and expression of the Salmonella enterotoxin gene. J Bacteriol. 1987 Nov;169(11):5095–5100. doi: 10.1128/jb.169.11.5095-5100.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Danbara H., Moriguchi R., Suzuki S., Tamura Y., Kijima M., Oishi K., Matsui H., Abe A., Nakamura M. Effect of 50 kilobase-plasmid, pKDSC50, of Salmonella choleraesuis RF-1 strain on pig septicemia. J Vet Med Sci. 1992 Dec;54(6):1175–1178. doi: 10.1292/jvms.54.1175. [DOI] [PubMed] [Google Scholar]
  6. Gulig P. A., Doyle T. J. The Salmonella typhimurium virulence plasmid increases the growth rate of salmonellae in mice. Infect Immun. 1993 Feb;61(2):504–511. doi: 10.1128/iai.61.2.504-511.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Heffernan E. J., Fierer J., Chikami G., Guiney D. Natural history of oral Salmonella dublin infection in BALB/c mice: effect of an 80-kilobase-pair plasmid on virulence. J Infect Dis. 1987 Jun;155(6):1254–1259. doi: 10.1093/infdis/155.6.1254. [DOI] [PubMed] [Google Scholar]
  8. Jones P. W. The effect of storage in slurry on the virulence of Salmonella dublin. J Hyg (Lond) 1975 Feb;74(1):65–70. doi: 10.1017/s0022172400046726. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Kapperud G., Gustavsen S., Hellesnes I., Hansen A. H., Lassen J., Hirn J., Jahkola M., Montenegro M. A., Helmuth R. Outbreak of Salmonella typhimurium infection traced to contaminated chocolate and caused by a strain lacking the 60-megadalton virulence plasmid. J Clin Microbiol. 1990 Dec;28(12):2597–2601. doi: 10.1128/jcm.28.12.2597-2601.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Koupal L. R., Deibel R. H. Assay, characterization, and localization of an enterotoxin produced by Salmonella. Infect Immun. 1975 Jan;11(1):14–22. doi: 10.1128/iai.11.1.14-22.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  12. Manning E. J., Baird G. D., Jones P. W. The role of plasmid genes in the pathogenicity of Salmonella dublin. J Med Microbiol. 1986 May;21(3):239–243. doi: 10.1099/00222615-21-3-239. [DOI] [PubMed] [Google Scholar]
  13. Pardon P., Popoff M. Y., Coynault C., Marly J., Miras I. Virulence-associated plasmids of Salmonella serotype Typhimurium in experimental murine infection. Ann Inst Pasteur Microbiol. 1986 Jul-Aug;137B(1):47–60. doi: 10.1016/s0769-2609(86)80093-x. [DOI] [PubMed] [Google Scholar]
  14. Riikonen P., Mäkelä P. H., Saarilahti H., Sukupolvi S., Taira S., Rhen M. The virulence plasmid does not contribute to growth of Salmonella in cultured murine macrophages. Microb Pathog. 1992 Oct;13(4):281–291. doi: 10.1016/0882-4010(92)90038-p. [DOI] [PubMed] [Google Scholar]
  15. Sedlock D. M., Deibel R. H. Detection of Salmonella enterotoxin using rabbit ileal loops. Can J Microbiol. 1978 Mar;24(3):268–273. doi: 10.1139/m78-046. [DOI] [PubMed] [Google Scholar]
  16. Threlfall E. J., Hampton M. D., Chart H., Rowe B. Use of plasmid profile typing for surveillance of Salmonella enteritidis phage type 4 from humans, poultry and eggs. Epidemiol Infect. 1994 Feb;112(1):25–31. doi: 10.1017/s0950268800057381. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Trucksis M., Galen J. E., Michalski J., Fasano A., Kaper J. B. Accessory cholera enterotoxin (Ace), the third toxin of a Vibrio cholerae virulence cassette. Proc Natl Acad Sci U S A. 1993 Jun 1;90(11):5267–5271. doi: 10.1073/pnas.90.11.5267. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Valone S. E., Chikami G. K., Miller V. L. Stress induction of the virulence proteins (SpvA, -B, and -C) from native plasmid pSDL2 of Salmonella dublin. Infect Immun. 1993 Feb;61(2):705–713. doi: 10.1128/iai.61.2.705-713.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Vandenbosch J. L., Kurlandsky D. R., Urdangaray R., Jones G. W. Evidence of coordinate regulation of virulence in Salmonella typhimurium involving the rsk element of the 95-kilobase plasmid. Infect Immun. 1989 Aug;57(8):2566–2568. doi: 10.1128/iai.57.8.2566-2568.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Wallis T. S., Hawker R. J., Candy D. C., Qi G. M., Clarke G. J., Worton K. J., Osborne M. P., Stephen J. Quantification of the leucocyte influx into rabbit ileal loops induced by strains of Salmonella typhimurium of different virulence. J Med Microbiol. 1989 Oct;30(2):149–156. doi: 10.1099/00222615-30-2-149. [DOI] [PubMed] [Google Scholar]
  21. Wallis T. S., Starkey W. G., Stephen J., Haddon S. J., Osborne M. P., Candy D. C. Enterotoxin production by Salmonella typhimurium strains of different virulence. J Med Microbiol. 1986 Feb;21(1):19–23. doi: 10.1099/00222615-21-1-19. [DOI] [PubMed] [Google Scholar]
  22. Wallis T. S., Vaughan A. T., Clarke G. J., Qi G. M., Worton K. J., Candy D. C., Osborne M. P., Stephen J. The role of leucocytes in the induction of fluid secretion by Salmonella typhimurium. J Med Microbiol. 1990 Jan;31(1):27–35. doi: 10.1099/00222615-31-1-27. [DOI] [PubMed] [Google Scholar]
  23. Watson P. R., Paulin S. M., Bland A. P., Jones P. W., Wallis T. S. Characterization of intestinal invasion by Salmonella typhimurium and Salmonella dublin and effect of a mutation in the invH gene. Infect Immun. 1995 Jul;63(7):2743–2754. doi: 10.1128/iai.63.7.2743-2754.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Williamson C. M., Baird G. D., Manning E. J. A common virulence region on plasmids from eleven serotypes of Salmonella. J Gen Microbiol. 1988 Apr;134(4):975–982. doi: 10.1099/00221287-134-4-975. [DOI] [PubMed] [Google Scholar]
  25. Williamson C. M., Pullinger G. D., Lax A. J. Identification of an essential virulence region on Salmonella plasmids. Microb Pathog. 1988 Dec;5(6):469–473. doi: 10.1016/0882-4010(88)90008-3. [DOI] [PubMed] [Google Scholar]
  26. Woodward M. J., McLaren I., Wray C. Distribution of virulence plasmids within Salmonellae. J Gen Microbiol. 1989 Mar;135(3):503–511. doi: 10.1099/00221287-135-3-503. [DOI] [PubMed] [Google Scholar]
  27. Yang M. K., Tan M. S. Characterization and cloning of enterotoxin genes of Salmonella typhimurium. Proc Natl Sci Counc Repub China B. 1989 Apr;13(2):109–118. [PubMed] [Google Scholar]

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