Skip to main content
Infection and Immunity logoLink to Infection and Immunity
. 1997 Apr;65(4):1267–1272. doi: 10.1128/iai.65.4.1267-1272.1997

Naturally occurring deletions in the centisome 63 pathogenicity island of environmental isolates of Salmonella spp.

C C Ginocchio 1, K Rahn 1, R C Clarke 1, J E Galán 1
PMCID: PMC175127  PMID: 9119461

Abstract

We have identified several environmental isolates of Salmonella senftenberg and S. litchfield which carry a deletion encompassing a vast segment of the centisome 63 region of the Salmonella chromosome. The deletion includes the entire inv, spa, and hil loci, which are required for entry of Salmonella spp. into mammalian cells. Consequently, these isolates were found to be markedly deficient in the ability to enter cultured epithelial cells. In contrast, no deletions were found in the corresponding regions of the chromosomes of clinical isolates of these serovars; consequently, these isolates were found to be highly invasive for cultured epithelial cells. These data confirm the importance of the centisome 63 region of the Salmonella chromosome in mediating the entry of these organisms into cultured mammalian cells and indicate that additional entry pathways are presumably not utilized by these environmental isolates. These results are also consistent with the notion that this region constitutes a pathogenicity island which remains unstable in certain Salmonella serotypes.

Full Text

The Full Text of this article is available as a PDF (315.6 KB).

Selected References

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

  1. Altmeyer R. M., McNern J. K., Bossio J. C., Rosenshine I., Finlay B. B., Galán J. E. Cloning and molecular characterization of a gene involved in Salmonella adherence and invasion of cultured epithelial cells. Mol Microbiol. 1993 Jan;7(1):89–98. doi: 10.1111/j.1365-2958.1993.tb01100.x. [DOI] [PubMed] [Google Scholar]
  2. Bliska J. B., Copass M. C., Falkow S. The Yersinia pseudotuberculosis adhesin YadA mediates intimate bacterial attachment to and entry into HEp-2 cells. Infect Immun. 1993 Sep;61(9):3914–3921. doi: 10.1128/iai.61.9.3914-3921.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Blum G., Ott M., Lischewski A., Ritter A., Imrich H., Tschäpe H., Hacker J. Excision of large DNA regions termed pathogenicity islands from tRNA-specific loci in the chromosome of an Escherichia coli wild-type pathogen. Infect Immun. 1994 Feb;62(2):606–614. doi: 10.1128/iai.62.2.606-614.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Collazo C. M., Galán J. E. Requirement for exported proteins in secretion through the invasion-associated type III system of Salmonella typhimurium. Infect Immun. 1996 Sep;64(9):3524–3531. doi: 10.1128/iai.64.9.3524-3531.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Collazo C. M., Zierler M. K., Galán J. E. Functional analysis of the Salmonella typhimurium invasion genes invl and invJ and identification of a target of the protein secretion apparatus encoded in the inv locus. Mol Microbiol. 1995 Jan;15(1):25–38. doi: 10.1111/j.1365-2958.1995.tb02218.x. [DOI] [PubMed] [Google Scholar]
  6. Eichelberg K., Ginocchio C. C., Galán J. E. Molecular and functional characterization of the Salmonella typhimurium invasion genes invB and invC: homology of InvC to the F0F1 ATPase family of proteins. J Bacteriol. 1994 Aug;176(15):4501–4510. doi: 10.1128/jb.176.15.4501-4510.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fetherston J. D., Schuetze P., Perry R. D. Loss of the pigmentation phenotype in Yersinia pestis is due to the spontaneous deletion of 102 kb of chromosomal DNA which is flanked by a repetitive element. Mol Microbiol. 1992 Sep;6(18):2693–2704. doi: 10.1111/j.1365-2958.1992.tb01446.x. [DOI] [PubMed] [Google Scholar]
  8. Galán J. E., Curtiss R., 3rd Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci U S A. 1989 Aug;86(16):6383–6387. doi: 10.1073/pnas.86.16.6383. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Galán J. E., Curtiss R., 3rd Distribution of the invA, -B, -C, and -D genes of Salmonella typhimurium among other Salmonella serovars: invA mutants of Salmonella typhi are deficient for entry into mammalian cells. Infect Immun. 1991 Sep;59(9):2901–2908. doi: 10.1128/iai.59.9.2901-2908.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Galán J. E., Ginocchio C., Costeas P. Molecular and functional characterization of the Salmonella invasion gene invA: homology of InvA to members of a new protein family. J Bacteriol. 1992 Jul;174(13):4338–4349. doi: 10.1128/jb.174.13.4338-4349.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Galán J. E. Molecular and cellular bases of Salmonella entry into host cells. Curr Top Microbiol Immunol. 1996;209:43–60. doi: 10.1007/978-3-642-85216-9_3. [DOI] [PubMed] [Google Scholar]
  12. Galán J. E. Molecular genetic bases of Salmonella entry into host cells. Mol Microbiol. 1996 Apr;20(2):263–271. doi: 10.1111/j.1365-2958.1996.tb02615.x. [DOI] [PubMed] [Google Scholar]
  13. Ginocchio C., Pace J., Galán J. E. Identification and molecular characterization of a Salmonella typhimurium gene involved in triggering the internalization of salmonellae into cultured epithelial cells. Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):5976–5980. doi: 10.1073/pnas.89.13.5976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Gouin E., Mengaud J., Cossart P. The virulence gene cluster of Listeria monocytogenes is also present in Listeria ivanovii, an animal pathogen, and Listeria seeligeri, a nonpathogenic species. Infect Immun. 1994 Aug;62(8):3550–3553. doi: 10.1128/iai.62.8.3550-3553.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kaniga K., Bossio J. C., Galán J. E. The Salmonella typhimurium invasion genes invF and invG encode homologues of the AraC and PulD family of proteins. Mol Microbiol. 1994 Aug;13(4):555–568. doi: 10.1111/j.1365-2958.1994.tb00450.x. [DOI] [PubMed] [Google Scholar]
  16. Knapp S., Hacker J., Jarchau T., Goebel W. Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol. 1986 Oct;168(1):22–30. doi: 10.1128/jb.168.1.22-30.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lawrence J. G., Roth J. R. Selfish operons: horizontal transfer may drive the evolution of gene clusters. Genetics. 1996 Aug;143(4):1843–1860. doi: 10.1093/genetics/143.4.1843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Low D., David V., Lark D., Schoolnik G., Falkow S. Gene clusters governing the production of hemolysin and mannose-resistant hemagglutination are closely linked in Escherichia coli serotype O4 and O6 isolates from urinary tract infections. Infect Immun. 1984 Jan;43(1):353–358. doi: 10.1128/iai.43.1.353-358.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. McDaniel T. K., Jarvis K. G., Donnenberg M. S., Kaper J. B. A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci U S A. 1995 Feb 28;92(5):1664–1668. doi: 10.1073/pnas.92.5.1664. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Miller V. L., Falkow S. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells. Infect Immun. 1988 May;56(5):1242–1248. doi: 10.1128/iai.56.5.1242-1248.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mills D. M., Bajaj V., Lee C. A. A 40 kb chromosomal fragment encoding Salmonella typhimurium invasion genes is absent from the corresponding region of the Escherichia coli K-12 chromosome. Mol Microbiol. 1995 Feb;15(4):749–759. doi: 10.1111/j.1365-2958.1995.tb02382.x. [DOI] [PubMed] [Google Scholar]
  22. Ochman H., Soncini F. C., Solomon F., Groisman E. A. Identification of a pathogenicity island required for Salmonella survival in host cells. Proc Natl Acad Sci U S A. 1996 Jul 23;93(15):7800–7804. doi: 10.1073/pnas.93.15.7800. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Pang P. P., Lundberg A. S., Walker G. C. Identification and characterization of the mutL and mutS gene products of Salmonella typhimurium LT2. J Bacteriol. 1985 Sep;163(3):1007–1015. doi: 10.1128/jb.163.3.1007-1015.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Rahn K., De Grandis S. A., Clarke R. C., McEwen S. A., Galán J. E., Ginocchio C., Curtiss R., 3rd, Gyles C. L. Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol Cell Probes. 1992 Aug;6(4):271–279. doi: 10.1016/0890-8508(92)90002-f. [DOI] [PubMed] [Google Scholar]
  25. SCHNEIDER H. A., ZINDER N. D. Nutrition of the host and natural resistance to infection. V. An improved assay employing genetic markers in the double strain inoculation test. J Exp Med. 1956 Feb 1;103(2):207–223. doi: 10.1084/jem.103.2.207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Shea J. E., Hensel M., Gleeson C., Holden D. W. Identification of a virulence locus encoding a second type III secretion system in Salmonella typhimurium. Proc Natl Acad Sci U S A. 1996 Mar 19;93(6):2593–2597. doi: 10.1073/pnas.93.6.2593. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Sheehan B., Kocks C., Dramsi S., Gouin E., Klarsfeld A. D., Mengaud J., Cossart P. Molecular and genetic determinants of the Listeria monocytogenes infectious process. Curr Top Microbiol Immunol. 1994;192:187–216. doi: 10.1007/978-3-642-78624-2_9. [DOI] [PubMed] [Google Scholar]
  28. Yang Y., Isberg R. R. Cellular internalization in the absence of invasin expression is promoted by the Yersinia pseudotuberculosis yadA product. Infect Immun. 1993 Sep;61(9):3907–3913. doi: 10.1128/iai.61.9.3907-3913.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]

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

RESOURCES