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PMID: 16672618 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Application of comparative phylogenomics to study the evolution of Yersinia enterocolitica and to identify genetic differences relating to pathogenicity.

Journal of bacteriology ·Vol. 188 ·No. 10 ·2006-05-00 ·Pages 3645-53

Howard SL, Gaunt MW, Hinds J, Witney AA, Stabler R, Wren BW

Abstract

Yersinia enterocolitica, an important cause of human gastroenteritis generally caused by the consumption of livestock, has traditionally been categorized into three groups with respect to pathogenicity, i.e., nonpathogenic (biotype 1A), low pathogenicity (biotypes 2 to 5), and highly pathogenic (biotype 1B). However, genetic differences that explain variation in pathogenesis and whether different biotypes are associated with specific nonhuman hosts are largely unknown. In this study, we applied comparative phylogenomics (whole-genome comparisons of microbes with DNA microarrays combined with Bayesian phylogenies) to investigate a diverse collection of 94 strains of Y. enterocolitica consisting of 35 human, 35 pig, 15 sheep, and 9 cattle isolates from nonpathogenic, low-pathogenicity, and highly pathogenic biotypes. Analysis confirmed three distinct statistically supported clusters composed of a nonpathogenic clade, a low-pathogenicity clade, and a highly pathogenic clade. Genetic differences revealed 125 predicted coding sequences (CDSs) present in all highly pathogenic strains but absent from the other clades. These included several previously uncharacterized CDSs that may encode novel virulence determinants including a hemolysin, a metalloprotease, and a type III secretion effector protein. Additionally, 27 CDSs were identified which were present in all 47 low-pathogenicity strains and Y. enterocolitica 8081 but absent from all nonpathogenic 1A isolates. Analysis of the core gene set for Y. enterocolitica revealed that 20.8% of the genes were shared by all of the strains, confirming this species as highly heterogeneous, adding to the case for the existence of three subspecies of Y. enterocolitica. Further analysis revealed that Y. enterocolitica does not cluster according to source (host).

MeSH Terms
Animals Bayes Theorem Evolution, Molecular Gastroenteritis/microbiology Genomics Humans Meat/microbiology Oligonucleotide Array Sequence Analysis Phylogeny Yersinia Infections/etiology Yersinia enterocolitica/classification,genetics,pathogenicity
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Howard Sarah L
Department of Infectious & Tropical Diseases, London School of Hygiene and Tropical Medicine, UK.
Gaunt Michael W
Hinds Jason
Witney Adam A
Stabler Richard
Wren Brendan W
References (57)
57 references, click to expand
  1. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic.
    Proc Natl Acad Sci U S A. 2001 Jul 17;98(15):8821-6 PMID: 11447287
  2. MRBAYES: Bayesian inference of phylogenetic trees.
    Bioinformatics. 2001 Aug;17(8):754-5 PMID: 11524383
  3. The epidemiology of Yersinia enterocolitica infection in the British Isles 1983-1988.
    Contrib Microbiol Immunol. 1991;12:17-25 PMID: 1935086
  4. Clinical significance of virulence-related assay of Yersinia species.
    J Clin Microbiol. 1987 May;25(5):802-7 PMID: 3584418
  5. The cytotoxic protein YopE of Yersinia obstructs the primary host defence.
    Mol Microbiol. 1990 Apr;4(4):657-67 PMID: 2191183
  6. Study of infectious intestinal disease in England: rates in the community, presenting to general practice, and reported to national surveillance. The Infectious Intestinal Disease Study Executive.
    BMJ. 1999 Apr 17;318(7190):1046-50 PMID: 10205103
  7. The Yersinia high-pathogenicity island.
    Int Microbiol. 1999 Sep;2(3):161-7 PMID: 10943409
  8. Improved analytical methods for microarray-based genome-composition analysis.
    Genome Biol. 2002 Oct 29;3(11):RESEARCH0065 PMID: 12429064
  9. Periplasmic copper-zinc superoxide dismutase of Legionella pneumophila: role in stationary-phase survival.
    J Bacteriol. 1996 Mar;178(6):1578-84 PMID: 8626284
  10. Correspondence of genotypes of sporadic Yersinia enterocolitica bioserotype 4/O:3 strains from human and porcine sources.
    Epidemiol Infect. 2001 Aug;127(1):37-47 PMID: 11561973
  11. Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K12 and O157.
    Nucleic Acids Res. 2002 Oct 15;30(20):4432-41 PMID: 12384590
  12. Association between clinical presentation, biogroups and virulence attributes of Yersinia enterocolitica strains in human diarrhoeal disease.
    Epidemiol Infect. 1996 Feb;116(1):27-34 PMID: 8626001
  13. Nonpathogenic isolates of Yersinia enterocolitica do not contain functional inv-homologous sequences.
    Infect Immun. 1990 Apr;58(4):1059-64 PMID: 1690684
  14. Identification of substrates and chaperone from the Yersinia enterocolitica 1B Ysa type III secretion system.
    Infect Immun. 2003 Jan;71(1):242-53 PMID: 12496172
  15. Primer3 on the WWW for general users and for biologist programmers.
    Methods Mol Biol. 2000;132:365-86 PMID: 10547847
  16. Plasmid-mediated tissue invasiveness in Yersinia enterocolitica.
    Nature. 1980 Jan 10;283(5743):224-6 PMID: 7350546
  17. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis.
    Proc Natl Acad Sci U S A. 2004 Sep 21;101(38):13826-31 PMID: 15358858
  18. Intracellular targeting of the Yersinia YopE cytotoxin in mammalian cells induces actin microfilament disruption.
    Infect Immun. 1991 Dec;59(12):4562-9 PMID: 1937815
  19. Bacterial [Cu,Zn]-cofactored superoxide dismutase protects opsonized, encapsulated Neisseria meningitidis from phagocytosis by human monocytes/macrophages.
    Infect Immun. 2003 Mar;71(3):1604-7 PMID: 12595487
  20. Identification and properties of the genes encoding microcin E492 and its immunity protein.
    J Bacteriol. 1999 Jan;181(1):212-7 PMID: 9864332
  21. Comparative phylogenomics of the food-borne pathogen Campylobacter jejuni reveals genetic markers predictive of infection source.
    Proc Natl Acad Sci U S A. 2005 Nov 1;102(44):16043-8 PMID: 16230626
  22. GSP-dependent protein secretion in gram-negative bacteria: the Xcp system of Pseudomonas aeruginosa.
    FEMS Microbiol Rev. 1998 Sep;22(3):177-98 PMID: 9818381
  23. The virulence plasmid pWR100 and the repertoire of proteins secreted by the type III secretion apparatus of Shigella flexneri.
    Mol Microbiol. 2000 Nov;38(4):760-71 PMID: 11115111
  24. Comparing genomes within the species Mycobacterium tuberculosis.
    Genome Res. 2001 Apr;11(4):547-54 PMID: 11282970
  25. Human and animal epidemic of Yersinia enterocolitica O:9, 1989-1997, Auvergne, France.
    Emerg Infect Dis. 1999 Sep-Oct;5(5):719-21 PMID: 10511531
  26. Comparative phylogenomics of pathogenic bacteria by microarray analysis.
    Curr Opin Microbiol. 2005 Oct;8(5):620-6 PMID: 16125441
  27. Yersinia enterocolitica: overview and epidemiologic correlates.
    Microbes Infect. 1999 Apr;1(4):323-33 PMID: 10602666
  28. Evidence for two genetic loci in Yersinia enterocolitica that can promote invasion of epithelial cells.
    Infect Immun. 1988 May;56(5):1242-8 PMID: 2833444
  29. Application of DNA microarrays to study the evolutionary genomics of Yersinia pestis and Yersinia pseudotuberculosis.
    Genome Res. 2003 Sep;13(9):2018-29 PMID: 12952873
  30. Characterization of plasmids and plasmid-associated determinants of Yersinia enterocolitica pathogenesis.
    Infect Immun. 1981 Feb;31(2):775-82 PMID: 7216474
  31. Novel virulence-associated type II secretion system unique to high-pathogenicity Yersinia enterocolitica.
    Infect Immun. 2003 Apr;71(4):1872-9 PMID: 12654803
  32. Yersinia enterocolitica infections and pork: the missing link.
    Lancet. 1987 May 16;1(8542):1129-32 PMID: 2883453
  33. A chromosomally encoded type III secretion pathway in Yersinia enterocolitica is important in virulence.
    Mol Microbiol. 2000 Jun;36(6):1436-46 PMID: 10931293
  34. Yersinia enterocolitica: the charisma continues.
    Clin Microbiol Rev. 1997 Apr;10(2):257-76 PMID: 9105754
  35. Whole genome comparison of Campylobacter jejuni human isolates using a low-cost microarray reveals extensive genetic diversity.
    Genome Res. 2001 Oct;11(10):1706-15 PMID: 11591647
  36. Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica.
    J Bacteriol. 1996 Dec;178(23):6743-51 PMID: 8955291
  37. Pathogenecity of Yersinia enterocolitica for mice.
    Infect Immun. 1975 Jan;11(1):164-70 PMID: 1116874
  38. MrBayes 3: Bayesian phylogenetic inference under mixed models.
    Bioinformatics. 2003 Aug 12;19(12):1572-4 PMID: 12912839
  39. cag, a pathogenicity island of Helicobacter pylori, encodes type I-specific and disease-associated virulence factors.
    Proc Natl Acad Sci U S A. 1996 Dec 10;93(25):14648-53 PMID: 8962108
  40. Yersinia pestis, the cause of plague, is a recently emerged clone of Yersinia pseudotuberculosis.
    Proc Natl Acad Sci U S A. 1999 Nov 23;96(24):14043-8 PMID: 10570195
  41. Transfer of the core region genes of the Yersinia enterocolitica WA-C serotype O:8 high-pathogenicity island to Y. enterocolitica MRS40, a strain with low levels of pathogenicity, confers a yersiniabactin biosynthesis phenotype and enhanced mouse virulence.
    Infect Immun. 2002 Apr;70(4):1832-41 PMID: 11895945
  42. Epidemiologic investigations of Yersinia enterocolitica and related species: sources, frequency, and serogroup distribution.
    J Clin Microbiol. 1990 May;28(5):910-2 PMID: 2351734
  43. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  44. The complete genome sequence of Chromobacterium violaceum reveals remarkable and exploitable bacterial adaptability.
    Proc Natl Acad Sci U S A. 2003 Sep 30;100(20):11660-5 PMID: 14500782
  45. Structural and functional consequences of cleavage of human secretory and human serum immunoglobulin A1 by proteinases from Proteus mirabilis and Neisseria meningitidis.
    Infect Immun. 2003 Jun;71(6):3349-56 PMID: 12761118
  46. Food-borne pathogens of recent concern.
    Annu Rev Nutr. 1985;5:25-41 PMID: 3927947
  47. Comparative genome analysis of Vibrio vulnificus, a marine pathogen.
    Genome Res. 2003 Dec;13(12):2577-87 PMID: 14656965
  48. From pig to pacifier: chitterling-associated yersiniosis outbreak among black infants.
    Emerg Infect Dis. 2003 Aug;9(8):1007-9 PMID: 12967503
  49. Yersinia enterocolitica 16S rRNA gene types belong to the same genospecies but form three homology groups.
    Int J Med Microbiol. 2000 Mar;290(1):61-4 PMID: 11043982
  50. The ail locus is found uniquely in Yersinia enterocolitica serotypes commonly associated with disease.
    Infect Immun. 1989 Jan;57(1):121-31 PMID: 2642465
  51. Comparison of the biotypes of Yersinia enterocolitica isolated from pigs, cattle and sheep at slaughter and from humans with yersiniosis in Great Britain during 1999-2000.
    Lett Appl Microbiol. 2004;39(1):103-8 PMID: 15189296
  52. Low occurrence of pathogenic Yersinia enterocolitica in clinical, food, and environmental samples: a methodological problem.
    Clin Microbiol Rev. 2003 Apr;16(2):220-9 PMID: 12692095
  53. Plasmid associated with pathogenicity and calcium dependency of Yersinia enterocolitica.
    Infect Immun. 1980 Feb;27(2):682-5 PMID: 7380546
  54. Desferrioxamine-promoted virulence of Yersinia enterocolitica in mice depends on both desferrioxamine type and mouse strain.
    J Infect Dis. 1994 Mar;169(3):562-7 PMID: 8158027
  55. Amino acid substitutions in naturally occurring variants of ail result in altered invasion activity.
    J Bacteriol. 1992 Feb;174(4):1360-9 PMID: 1370953
  56. Comparative genomic analysis of Vibrio cholerae: genes that correlate with cholera endemic and pandemic disease.
    Proc Natl Acad Sci U S A. 2002 Feb 5;99(3):1556-61 PMID: 11818571
  57. Pathogenicity of Yersinia enterocolitica biotype 1A.
    FEMS Immunol Med Microbiol. 2003 Sep 22;38(2):127-37 PMID: 13129647
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
2006-05-00
Pages
3645-53
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC1482848
Subset
IM
Grants
Wellcome Trust · United Kingdom
Wellcome Trust · 062511 · United Kingdom
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