Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1982 Nov;38(2):476–486. doi: 10.1128/iai.38.2.476-486.1982

Association of adhesive, invasive, and virulent phenotypes of Salmonella typhimurium with autonomous 60-megadalton plasmids.

G W Jones, D K Rabert, D M Svinarich, H J Whitfield
PMCID: PMC347764  PMID: 6128304

Abstract

The plasmid DNA content of six invasive and adhesive strains of Salmonella typhimurium was determined, and all six strains (CR8500 [S850], CR6600 [TML], W118, NY, PR, and S2204) were found to harbor at least one plasmid equivalent in size to the 60-megadalton plasmid ("cryptic" plasmid), pSLT, which is normally resident in S. typhimurium strain LT2. The role of such 60-megadalton plasmids in the adhesive and invasive properties of strain CR6600, a commonly encountered salmonella pathogen that produces type 1 fimbriae, and strain CR8500, a representative FIRN biotype which does not produce type 1 fimbriae, was studied further by obtaining derivatives of these strains that no longer harbored an autonomous 60-megadalton plasmid. Strains CR6260 and CR6190 and strains CR8100 and CR8353, which were "cured" derivatives of strains CR6600 and CR8500, respectively, were significantly less adhesive and invasive in the HeLa cell test. A 53.5-megadalton colicin plasmid harbored by strain CR6600 did not detectably influence these properties. Additionally, strain CR6260 was avirulent, and strain CR8100 was 1,000 to 10,000-fold less virulent for orally infected mice as compared with their respective parental strains. Significantly, the virulence of strain CR8100 correlated with tissue colonization by bacteria that exhibited autonomous copies of a 60-megadalton plasmid. We propose that this plasmid exists in both autonomous and integrated states and that the in vivo environment selects for bacteria with autonomous plasmid copies which can express the virulent phenotype, thus enabling such strains to survive the defense mechanisms of the host.

Full text

PDF
476

Images in this article

480Image
on p.480
480Image
on p.480
481Image
on p.481
483Image
on p.483

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bagdasarian M., Hryniewicz M., Zdzienicka M. Integrative suppression of a dnaA mutation in Salmonella typhimurium. Mol Gen Genet. 1975 Aug 27;139(3):213–231. doi: 10.1007/BF00268973. [DOI] [PubMed] [Google Scholar]
  2. Bendler J. W., 3rd Physical size of the donor locus and transmission of Haemophilus influenzae ampicillin resistance genes by deoxyribonucleic acid-mediated transformation. J Bacteriol. 1976 Jan;125(1):197–204. doi: 10.1128/jb.125.1.197-204.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berg R. D. Mechanisms confining indigenous bacteria to the gastrointestinal tract. Am J Clin Nutr. 1980 Nov;33(11 Suppl):2472–2484. doi: 10.1093/ajcn/33.11.2472. [DOI] [PubMed] [Google Scholar]
  4. Bochner B. R., Huang H. C., Schieven G. L., Ames B. N. Positive selection for loss of tetracycline resistance. J Bacteriol. 1980 Aug;143(2):926–933. doi: 10.1128/jb.143.2.926-933.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bouanchaud D. H., Scavizzi M. R., Chabbert Y. A. Elimination by ethidium bromide of antibiotic resistance in enterobacteria and staphylococci. J Gen Microbiol. 1968 Dec;54(3):417–425. doi: 10.1099/00221287-54-3-417. [DOI] [PubMed] [Google Scholar]
  6. Clancy J., Savage D. C. Another Colicin V phenotype: in vitro adhesion of Escherichia coli to mouse intestinal epithelium. Infect Immun. 1981 Apr;32(1):343–352. doi: 10.1128/iai.32.1.343-352.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Clowes R. C. Molecular structure of bacterial plasmids. Bacteriol Rev. 1972 Sep;36(3):361–405. doi: 10.1128/br.36.3.361-405.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Dowman J. E., Meynell G. G. Pleiotropic effects of de-repressed bacterial sex factors on colicinogeny and cell wall structure. Mol Gen Genet. 1970;109(1):57–68. doi: 10.1007/BF00334046. [DOI] [PubMed] [Google Scholar]
  9. Duguid J. P., Anderson E. S., Alfredsson G. A., Barker R., Old D. C. A new biotyping scheme for Salmonella typhimurium and its phylogenetic significance. J Med Microbiol. 1975 Feb;8(1):149–166. doi: 10.1099/00222615-8-1-149. [DOI] [PubMed] [Google Scholar]
  10. Duguid J. P., Darekar M. R., Wheater D. W. Fimbriae and infectivity in Salmonella typhimurium. J Med Microbiol. 1976 Nov;9(4):459–473. doi: 10.1099/00222615-9-4-459. [DOI] [PubMed] [Google Scholar]
  11. Elwell L. P., Shipley P. L. Plasmid-mediated factors associated with virulence of bacteria to animals. Annu Rev Microbiol. 1980;34:465–496. doi: 10.1146/annurev.mi.34.100180.002341. [DOI] [PubMed] [Google Scholar]
  12. Gemski P., Lazere J. R., Casey T. Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica. Infect Immun. 1980 Feb;27(2):682–685. doi: 10.1128/iai.27.2.682-685.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gemski P., Lazere J. R., Casey T., Wohlhieter J. A. Presence of a virulence-associated plasmid in Yersinia pseudotuberculosis. Infect Immun. 1980 Jun;28(3):1044–1047. doi: 10.1128/iai.28.3.1044-1047.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Giannella R. A., Washington O., Gemski P., Formal S. B. Invasion of HeLa cells by Salmonella typhimurium: a model for study of invasiveness of Salmonella. J Infect Dis. 1973 Jul;128(1):69–75. doi: 10.1093/infdis/128.1.69. [DOI] [PubMed] [Google Scholar]
  15. Graham A. C., Stocker B. A. Genetics of sensitivity of Salmonella species to colicin M and bacteriophages T5, T1, and ES18. J Bacteriol. 1977 Jun;130(3):1214–1223. doi: 10.1128/jb.130.3.1214-1223.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Hartman P. E. Some improved methods in P22 transduction. Genetics. 1974 Apr;76(4):625–631. doi: 10.1093/genetics/76.4.625. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Jones G. W., Richardson L. A. The attachment to, and invasion of HeLa cells by Salmonella typhimurium: the contribution of mannose-sensitive and mannose-resistant haemagglutinating activities. J Gen Microbiol. 1981 Dec;127(2):361–370. doi: 10.1099/00221287-127-2-361. [DOI] [PubMed] [Google Scholar]
  18. Jones G. W., Richardson L. A., Uhlman D. The invasion of HeLa cells by Salmonella typhimurium: reversible and irreversible bacterial attachment and the role of bacterial motility. J Gen Microbiol. 1981 Dec;127(2):351–360. doi: 10.1099/00221287-127-2-351. [DOI] [PubMed] [Google Scholar]
  19. Kado C. I., Liu S. T. Rapid procedure for detection and isolation of large and small plasmids. J Bacteriol. 1981 Mar;145(3):1365–1373. doi: 10.1128/jb.145.3.1365-1373.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kehoe M. A., Foster T. J. Genetic analysis of mutations in the transfer genes of pDU202 tra::Tn10 plasmids, caused by the excision of Tn10. Mol Gen Genet. 1977 Nov 29;157(1):109–118. doi: 10.1007/BF00268693. [DOI] [PubMed] [Google Scholar]
  21. Kihlström E., Nilsson L. Endocytosis of Salmonella typhimurium 395 MS and MR10 by HeLa cells. Acta Pathol Microbiol Scand B. 1977 Oct;85B(5):322–328. doi: 10.1111/j.1699-0463.1977.tb01982.x. [DOI] [PubMed] [Google Scholar]
  22. Kleckner N. Translocatable elements in procaryotes. Cell. 1977 May;11(1):11–23. doi: 10.1016/0092-8674(77)90313-0. [DOI] [PubMed] [Google Scholar]
  23. Kopecko D. J., Holcombe J., Formal S. B. Molecular characterization of plasmids from virulent and spontaneously occurring avirulent colonial variants of Shigella flexneri. Infect Immun. 1979 May;24(2):580–582. doi: 10.1128/iai.24.2.580-582.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Macrina F. L., Kopecko D. J., Jones K. R., Ayers D. J., McCowen S. M. A multiple plasmid-containing Escherichia coli strain: convenient source of size reference plasmid molecules. Plasmid. 1978 Jun;1(3):417–420. doi: 10.1016/0147-619x(78)90056-2. [DOI] [PubMed] [Google Scholar]
  25. Manis J. J., Whitfield H. J. Physical characterization of a plasmid cointegrate containing an F'his gnd element and the Salmonella typhimurium LT2 cryptic plasmid. J Bacteriol. 1977 Mar;129(3):1601–1606. doi: 10.1128/jb.129.3.1601-1606.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. McHugh G. L., Swartz M. N. Elimination of plasmids from several bacterial species by novobiocin. Antimicrob Agents Chemother. 1977 Sep;12(3):423–426. doi: 10.1128/aac.12.3.423. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Portnoy D. A., Moseley S. L., Falkow S. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis. Infect Immun. 1981 Feb;31(2):775–782. doi: 10.1128/iai.31.2.775-782.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sanderson K. E., Hartman P. E. Linkage map of Salmonella typhimurium, edition V. Microbiol Rev. 1978 Jun;42(2):471–519. doi: 10.1128/mr.42.2.471-519.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sansonetti P. J., Kopecko D. J., Formal S. B. Involvement of a plasmid in the invasive ability of Shigella flexneri. Infect Immun. 1982 Mar;35(3):852–860. doi: 10.1128/iai.35.3.852-860.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sansonetti P. J., Kopecko D. J., Formal S. B. Shigella sonnei plasmids: evidence that a large plasmid is necessary for virulence. Infect Immun. 1981 Oct;34(1):75–83. doi: 10.1128/iai.34.1.75-83.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Smith H. R., Humphreys G. O., Grindley N. D., Grindley J. N., Anderson E. S. Molecular studies of an fi+ plasmid from strains of Salmonella typhimurium. Mol Gen Genet. 1973 Nov 2;126(2):143–151. doi: 10.1007/BF00330989. [DOI] [PubMed] [Google Scholar]
  32. Smith H. W. A search for transmissible pathogenic characters in invasive strains of Escherichia coli: the discovery of a plasmid-controlled toxin and a plasmid-controlled lethal character closely associated, or identical, with colicine V. J Gen Microbiol. 1974 Jul;83(0):95–111. doi: 10.1099/00221287-83-1-95. [DOI] [PubMed] [Google Scholar]
  33. Spratt B. G., Rowbury R. J. The plasmid of Salmonella typhimurium LT2. Mol Gen Genet. 1973 Mar 19;121(4):347–353. doi: 10.1007/BF00433233. [DOI] [PubMed] [Google Scholar]
  34. Stuy J. H. Chromosomally integrated conjugative plasmids are common in antibiotic-resistant Haemophilus influenzae. J Bacteriol. 1980 Jun;142(3):925–930. doi: 10.1128/jb.142.3.925-930.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Timmis K., Cabello F., Cohen S. N. Cloning, isolation, and characterization of replication regions of complex plasmid genomes. Proc Natl Acad Sci U S A. 1975 Jun;72(6):2242–2246. doi: 10.1073/pnas.72.6.2242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Tomoeda M., Inuzuka M., Kubo N., Nakamura S. Effective elimination of drug resistance and sex factors in Escherichia coli by sodium dodecyl sulfate. J Bacteriol. 1968 Mar;95(3):1078–1089. doi: 10.1128/jb.95.3.1078-1089.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Uhlman D. L., Jones G. W. Chemotaxis as a factor in interactions between HeLa cells and Salmonella typhimurium. J Gen Microbiol. 1982 Feb;128(2):415–418. doi: 10.1099/00221287-128-2-415. [DOI] [PubMed] [Google Scholar]
  38. Wilkinson R. G., Gemski P., Jr, Stocker B. A. Non-smooth mutants of Salmonella typhimurium: differentiation by phage sensitivity and genetic mapping. J Gen Microbiol. 1972 May;70(3):527–554. doi: 10.1099/00221287-70-3-527. [DOI] [PubMed] [Google Scholar]
  39. Williams P. H., Warner P. J. ColV plasmid-mediated, colicin V-independent iron uptake system of invasive strains of Escherichia coli. Infect Immun. 1980 Aug;29(2):411–416. doi: 10.1128/iai.29.2.411-416.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Zink D. L., Feeley J. C., Wells J. G., Vanderzant C., Vickery J. C., Roof W. D., O'Donovan G. A. Plasmid-mediated tissue invasiveness in Yersinia enterocolitica. Nature. 1980 Jan 10;283(5743):224–226. doi: 10.1038/283224a0. [DOI] [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES