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. 1996 Dec;178(23):6743–6751. doi: 10.1128/jb.178.23.6743-6751.1996

Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica.

E Carniel 1, I Guilvout 1, M Prentice 1
PMCID: PMC178570  PMID: 8955291

Abstract

Pathogenic Yersinia spp. can be subdivided into highly pathogenic (high-pathogenicity) and low-pathogenicity strains. Several genes specific for the high-pathogenicity strains are clustered on a chromosomal fragment designated a "high-pathogenicity island" (HPI). In the present work, the HPI of biotype 1B strain Ye 8081 of Y. enterocolitica was characterized. We demonstrate important differences from the HPI of Y. pestis. The HPI of Y. enterocolitica is smaller (45 kb) and is not flanked by insertion sequences. A copy of the gene coding for the tRNA-Asn is present at one extremity of the HPI and may, as in uropathogenic Escherichia coli, participate in the excision of the island. In addition to the genes encoding the yersiniabactin-pesticin receptor and the high-molecular-weight protein 2, four repeated sequences are present on the HPI of Y. enterocolitica. At least two of them are insertion elements: previously described IS1328 and newly characterized IS1400. Comparison of the HPI of strain Ye 8081 with that of other Y. enterocolitica strains of biotype 1B indicates that most of the island is conserved, apart from 15 kb at the left-hand end which is variable, especially in the region where three repeated sequences are clustered.

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Selected References

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

  1. Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
  2. BURROWS T. W., JACKSON S. The virulence-enhancing effect of iron on nonpigmented mutants of virulent strains of Pasteurella pestis. Br J Exp Pathol. 1956 Dec;37(6):577–583. [PMC free article] [PubMed] [Google Scholar]
  3. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. 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]
  5. Brubaker R. R. Mutation rate to nonpigmentation in Pasteurella pestis. J Bacteriol. 1969 Jun;98(3):1404–1406. doi: 10.1128/jb.98.3.1404-1406.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carniel E., Guiyoule A., Guilvout I., Mercereau-Puijalon O. Molecular cloning, iron-regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia. Mol Microbiol. 1992 Feb;6(3):379–388. doi: 10.1111/j.1365-2958.1992.tb01481.x. [DOI] [PubMed] [Google Scholar]
  7. Carniel E., Guiyoule A., Mercereau-Puijalon O., Mollaret H. H. Chromosomal marker for the 'high pathogenicity' phenotype in Yersinia. Contrib Microbiol Immunol. 1991;12:192–197. [PubMed] [Google Scholar]
  8. Carniel E., Mercereau-Puijalon O., Bonnefoy S. The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains. Infect Immun. 1989 Apr;57(4):1211–1217. doi: 10.1128/iai.57.4.1211-1217.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Cheetham B. F., Katz M. E. A role for bacteriophages in the evolution and transfer of bacterial virulence determinants. Mol Microbiol. 1995 Oct;18(2):201–208. doi: 10.1111/j.1365-2958.1995.mmi_18020201.x. [DOI] [PubMed] [Google Scholar]
  10. Fetherston J. D., Lillard J. W., Jr, Perry R. D. Analysis of the pesticin receptor from Yersinia pestis: role in iron-deficient growth and possible regulation by its siderophore. J Bacteriol. 1995 Apr;177(7):1824–1833. doi: 10.1128/jb.177.7.1824-1833.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Fetherston J. D., Perry R. D. The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2. Mol Microbiol. 1994 Aug;13(4):697–708. doi: 10.1111/j.1365-2958.1994.tb00463.x. [DOI] [PubMed] [Google Scholar]
  12. 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]
  13. Forsberg A., Wolf-Watz H. Genetic analysis of the yopE region of Yersinia spp.: identification of a novel conserved locus, yerA, regulating yopE expression. J Bacteriol. 1990 Mar;172(3):1547–1555. doi: 10.1128/jb.172.3.1547-1555.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Fournier M. J., Ozeki H. Structure and organization of the transfer ribonucleic acid genes of Escherichia coli K-12. Microbiol Rev. 1985 Dec;49(4):379–397. doi: 10.1128/mr.49.4.379-397.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Galyov E. E., Håkansson S., Wolf-Watz H. Characterization of the operon encoding the YpkA Ser/Thr protein kinase and the YopJ protein of Yersinia pseudotuberculosis. J Bacteriol. 1994 Aug;176(15):4543–4548. doi: 10.1128/jb.176.15.4543-4548.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Guilvout I., Mercereau-Puijalon O., Bonnefoy S., Pugsley A. P., Carniel E. High-molecular-weight protein 2 of Yersinia enterocolitica is homologous to AngR of Vibrio anguillarum and belongs to a family of proteins involved in nonribosomal peptide synthesis. J Bacteriol. 1993 Sep;175(17):5488–5504. doi: 10.1128/jb.175.17.5488-5504.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Hacker J., Bender L., Ott M., Wingender J., Lund B., Marre R., Goebel W. Deletions of chromosomal regions coding for fimbriae and hemolysins occur in vitro and in vivo in various extraintestinal Escherichia coli isolates. Microb Pathog. 1990 Mar;8(3):213–225. doi: 10.1016/0882-4010(90)90048-u. [DOI] [PubMed] [Google Scholar]
  18. Heesemann J., Hantke K., Vocke T., Saken E., Rakin A., Stojiljkovic I., Berner R. Virulence of Yersinia enterocolitica is closely associated with siderophore production, expression of an iron-repressible outer membrane polypeptide of 65,000 Da and pesticin sensitivity. Mol Microbiol. 1993 Apr;8(2):397–408. doi: 10.1111/j.1365-2958.1993.tb01583.x. [DOI] [PubMed] [Google Scholar]
  19. Kearney B., Staskawicz B. J. Characterization of IS476 and its role in bacterial spot disease of tomato and pepper. J Bacteriol. 1990 Jan;172(1):143–148. doi: 10.1128/jb.172.1.143-148.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Komine Y., Adachi T., Inokuchi H., Ozeki H. Genomic organization and physical mapping of the transfer RNA genes in Escherichia coli K12. J Mol Biol. 1990 Apr 20;212(4):579–598. doi: 10.1016/0022-2836(90)90224-A. [DOI] [PubMed] [Google Scholar]
  21. Krause M., Harwood J., Fierer J., Guiney D. Genetic analysis of homology between the virulence plasmids of Salmonella dublin and Yersinia pseudotuberculosis. Infect Immun. 1991 May;59(5):1860–1863. doi: 10.1128/iai.59.5.1860-1863.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Labigne-Roussel A., Courcoux P., Tompkins L. Gene disruption and replacement as a feasible approach for mutagenesis of Campylobacter jejuni. J Bacteriol. 1988 Apr;170(4):1704–1708. doi: 10.1128/jb.170.4.1704-1708.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Marck C. 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 1988 Mar 11;16(5):1829–1836. doi: 10.1093/nar/16.5.1829. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Michiels T., Vanooteghem J. C., Lambert de Rouvroit C., China B., Gustin A., Boudry P., Cornelis G. R. Analysis of virC, an operon involved in the secretion of Yop proteins by Yersinia enterocolitica. J Bacteriol. 1991 Aug;173(16):4994–5009. doi: 10.1128/jb.173.16.4994-5009.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Michiels T., Wattiau P., Brasseur R., Ruysschaert J. M., Cornelis G. Secretion of Yop proteins by Yersiniae. Infect Immun. 1990 Sep;58(9):2840–2849. doi: 10.1128/iai.58.9.2840-2849.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Miller V. L., Bliska J. B., Falkow S. Nucleotide sequence of the Yersinia enterocolitica ail gene and characterization of the Ail protein product. J Bacteriol. 1990 Feb;172(2):1062–1069. doi: 10.1128/jb.172.2.1062-1069.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Perry R. D., Pendrak M. L., Schuetze P. Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis. J Bacteriol. 1990 Oct;172(10):5929–5937. doi: 10.1128/jb.172.10.5929-5937.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Podladchikova O. N., Dikhanov G. G., Rakin A. V., Heesemann J. Nucleotide sequence and structural organization of Yersinia pestis insertion sequence IS100. FEMS Microbiol Lett. 1994 Sep 1;121(3):269–274. doi: 10.1111/j.1574-6968.1994.tb07111.x. [DOI] [PubMed] [Google Scholar]
  30. Polard P., Prère M. F., Chandler M., Fayet O. Programmed translational frameshifting and initiation at an AUU codon in gene expression of bacterial insertion sequence IS911. J Mol Biol. 1991 Dec 5;222(3):465–477. doi: 10.1016/0022-2836(91)90490-w. [DOI] [PubMed] [Google Scholar]
  31. Priefer U. B., Kalinowski J., Rüger B., Heumann W., Pühler A. ISR1, a transposable DNA sequence resident in Rhizobium class IV strains, shows structural characteristics of classical insertion elements. Plasmid. 1989 Mar;21(2):120–128. doi: 10.1016/0147-619x(89)90055-3. [DOI] [PubMed] [Google Scholar]
  32. Prère M. F., Chandler M., Fayet O. Transposition in Shigella dysenteriae: isolation and analysis of IS911, a new member of the IS3 group of insertion sequences. J Bacteriol. 1990 Jul;172(7):4090–4099. doi: 10.1128/jb.172.7.4090-4099.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Rakin A., Heesemann J. Virulence-associated fyuA/irp2 gene cluster of Yersinia enterocolitica biotype 1B carries a novel insertion sequence IS1328. FEMS Microbiol Lett. 1995 Jun 15;129(2-3):287–292. doi: 10.1111/j.1574-6968.1995.tb07594.x. [DOI] [PubMed] [Google Scholar]
  34. Rakin A., Saken E., Harmsen D., Heesemann J. The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function. Mol Microbiol. 1994 Jul;13(2):253–263. doi: 10.1111/j.1365-2958.1994.tb00420.x. [DOI] [PubMed] [Google Scholar]
  35. Rimpiläinen M., Forsberg A., Wolf-Watz H. A novel protein, LcrQ, involved in the low-calcium response of Yersinia pseudotuberculosis shows extensive homology to YopH. J Bacteriol. 1992 May;174(10):3355–3363. doi: 10.1128/jb.174.10.3355-3363.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Robins-Browne R. M., Prpic J. K. Effects of iron and desferrioxamine on infections with Yersinia enterocolitica. Infect Immun. 1985 Mar;47(3):774–779. doi: 10.1128/iai.47.3.774-779.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Schwartz E., Kröger M., Rak B. IS150: distribution, nucleotide sequence and phylogenetic relationships of a new E. coli insertion element. Nucleic Acids Res. 1988 Jul 25;16(14B):6789–6802. doi: 10.1093/nar/16.14.6789. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Simonet M., Riot B., Fortineau N., Berche P. Invasin production by Yersinia pestis is abolished by insertion of an IS200-like element within the inv gene. Infect Immun. 1996 Jan;64(1):375–379. doi: 10.1128/iai.64.1.375-379.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Skurnik M., Toivanen P. Intervening sequences (IVSs) in the 23S ribosomal RNA genes of pathogenic Yersinia enterocolitica strains. The IVSs in Y. enterocolitica and Salmonella typhimurium have a common origin. Mol Microbiol. 1991 Mar;5(3):585–593. doi: 10.1111/j.1365-2958.1991.tb00729.x. [DOI] [PubMed] [Google Scholar]
  40. Skurnik M., Wolf-Watz H. Analysis of the yopA gene encoding the Yop1 virulence determinants of Yersinia spp. Mol Microbiol. 1989 Apr;3(4):517–529. doi: 10.1111/j.1365-2958.1989.tb00198.x. [DOI] [PubMed] [Google Scholar]
  41. Staden R. A computer program to search for tRNA genes. Nucleic Acids Res. 1980 Feb 25;8(4):817–825. [PMC free article] [PubMed] [Google Scholar]
  42. Surgalla M. J., Beesley E. D. Congo red-agar plating medium for detecting pigmentation in Pasteurella pestis. Appl Microbiol. 1969 Nov;18(5):834–837. doi: 10.1128/am.18.5.834-837.1969. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Van Gijsegem F., Gough C., Zischek C., Niqueux E., Arlat M., Genin S., Barberis P., German S., Castello P., Boucher C. The hrp gene locus of Pseudomonas solanacearum, which controls the production of a type III secretion system, encodes eight proteins related to components of the bacterial flagellar biogenesis complex. Mol Microbiol. 1995 Mar;15(6):1095–1114. doi: 10.1111/j.1365-2958.1995.tb02284.x. [DOI] [PubMed] [Google Scholar]
  44. Wood M. S., Byrne A., Lessie T. G. IS406 and IS407, two gene-activating insertion sequences for Pseudomonas cepacia. Gene. 1991 Aug 30;105(1):101–105. doi: 10.1016/0378-1119(91)90519-h. [DOI] [PubMed] [Google Scholar]
  45. de Almeida A. M., Guiyoule A., Guilvout I., Iteman I., Baranton G., Carniel E. Chromosomal irp2 gene in Yersinia: distribution, expression, deletion and impact on virulence. Microb Pathog. 1993 Jan;14(1):9–21. doi: 10.1006/mpat.1993.1002. [DOI] [PubMed] [Google Scholar]

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