Prevalence of the “High-Pathogenicity Island” of Yersinia Species among Escherichia coliStrains That Are Pathogenic to Humans

ABSTRACT The fyuA-irp gene cluster contributes to the virulence of highly pathogenic Yersinia (Yersinia pestis,Yersinia pseudotuberculosis, and Yersinia enterocolitica 1B). The cluster encodes an iron uptake system mediated by the siderophore yersiniabactin and reveals features of a pathogenicity island. Two evolutionary lineages of this “high pathogenicity island” (HPI) can be distinguished on the basis of DNA sequence comparison: a Y. pestis group and a Y. enterocolitica group. In this study we demonstrate that the HPI of the Y. pestis evolutionary group is disseminated among species of the family Enterobacteriaceae which are pathogenic to humans. It prevails in enteroaggregativeEscherichia coli and in E. coli blood culture isolates (93 and 80%, respectively), but is rarely found in enteropathogenic E. coli, enteroinvasive E. coli, and enterotoxigenic E. coli isolates. In contrast, the HPI was absent from enterohemorrhagic E. coli, Shigella, and Salmonella entericastrains investigated. Polypeptides encoded by the fyuA,irp1, and irp2 genes located on the HPI could be detected in E. coli strains pathogenic to humans. However, these E. coli strains showed a reduced sensitivity to the bacteriocin pesticin, whose uptake is mediated by the FyuA receptor. Escherichia strains do not possess thehms gene locus thought to be a part of the HPI of Y. pestis. Deletions of the fyuA-irp gene cluster affecting solely the fyuA part of the HPI were identified in 3% of the E. coli strains tested. These results suggest horizontal transfer of the HPI between Y. pestis and some pathogenic E. coli strains.

[1]  I. Henderson,et al.  Phylogenetic Analysis of Enteroaggregative and Diffusely Adherent Escherichia coli , 1999, Infection and Immunity.

[2]  J. Heesemann,et al.  The Yersiniabactin Biosynthetic Gene Cluster of Yersinia enterocolitica: Organization and Siderophore-Dependent Regulation , 1998, Journal of bacteriology.

[3]  H. Karch,et al.  Acute and chronic diarrhoea and abdominal colic associated with enteroaggregative Escherichia coli in young children living in western Europe , 1997, The Lancet.

[4]  R. Perry,et al.  Genetic organization of the yersiniabactin biosynthetic region and construction of avirulent mutants in Yersinia pestis , 1997, Infection and immunity.

[5]  M. Prentice,et al.  Characterization of a large chromosomal "high-pathogenicity island" in biotype 1B Yersinia enterocolitica , 1996, Journal of bacteriology.

[6]  M. Ikebe Contractile Mechanisms. (Book Reviews: Biochemistry of Smooth Muscle Contraction.) , 1996 .

[7]  T. Lucier,et al.  Iron uptake and iron-repressible polypeptides in Yersinia pestis , 1996, Infection and immunity.

[8]  T. Schwan,et al.  Role of the Yersinia pestis Hemin Storage (hms) Locus in the Transmission of Plague by Fleas , 1996, Science.

[9]  J. Heesemann,et al.  Virulence-associated fyuA/irp2 gene cluster of Yersinia enterocolitica biotype 1B carries a novel insertion sequence IS1328. , 1995, FEMS microbiology letters.

[10]  J. Heesemann,et al.  Evidence for two evolutionary lineages of highly pathogenic Yersinia species , 1995, Journal of bacteriology.

[11]  J. Heesemann,et al.  Development of PCR for screening of enteroaggregative Escherichia coli , 1995, Journal of clinical microbiology.

[12]  L. Beutin,et al.  Nucleotide sequence analysis of enteropathogenic Escherichia coli (EPEC) adherence factor probe and development of PCR for rapid detection of EPEC harboring virulence plasmids , 1994, Journal of clinical microbiology.

[13]  R. Perry,et al.  The pigmentation locus of Yersinia pestis KIM6+ is flanked by an insertion sequence and includes the structural genes for pesticin sensitivity and HMWP2 , 1994, Molecular microbiology.

[14]  H. Karch,et al.  Prevalence of attaching and effacing Escherichia coli in stool samples from patients and controls. , 1994, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[15]  J. Heesemann,et al.  The pesticin receptor of Yersinia enterocolitica: a novel virulence factor with dual function , 1994, Molecular Microbiology.

[16]  C. D. Cox,et al.  Pseudomonas siderophore pyochelin enhances neutrophil-mediated endothelial cell injury. , 1994, The American journal of physiology.

[17]  É. Carniel,et al.  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 , 1993, Journal of bacteriology.

[18]  R. Perry,et al.  Proteins essential for expression of the Hms+ phenotype of Yersinia pestis , 1993, Molecular microbiology.

[19]  J. Heesemann,et al.  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 , 1993, Molecular microbiology.

[20]  M. Kothary,et al.  Aggregative adherence fimbria I expression in enteroaggregative Escherichia coli requires two unlinked plasmid regions , 1993, Infection and immunity.

[21]  T. Lucier,et al.  Storage reservoirs of hemin and inorganic iron in Yersinia pestis , 1993, Infection and immunity.

[22]  G. Baranton,et al.  Chromosomal irp2 gene in Yersinia: distribution, expression, deletion and impact on virulence. , 1993, Microbial pathogenesis.

[23]  R. Perry,et al.  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 , 1992, Molecular microbiology.

[24]  D. Maneval,et al.  Aggregative adherence fimbriae I of enteroaggregative Escherichia coli mediate adherence to HEp-2 cells and hemagglutination of human erythrocytes , 1992, Infection and immunity.

[25]  É. Carniel,et al.  Molecular cloning, iron‐regulation and mutagenesis of the irp2 gene encoding HMWP2, a protein specific for the highly pathogenic Yersinia , 1992, Molecular microbiology.

[26]  T. Cheasty,et al.  Identification of enteropathogenic Escherichia coli isolated in Britain as enteroaggregative or as members of a subclass of attaching-and-effacing E. coli not hybridising with the EPEC adherence-factor probe. , 1991, Journal of medical microbiology.

[27]  R. Perry,et al.  Identification and cloning of a hemin storage locus involved in the pigmentation phenotype of Yersinia pestis , 1990, Journal of bacteriology.

[28]  G. Schoolnik,et al.  Detection of Shigella in feces using DNA amplification. , 1990, The Journal of infectious diseases.

[29]  M. Levine,et al.  Comparison of two assay methods for patterns of adherence to HEp-2 cells of Escherichia coli from patients with diarrhea , 1990, Journal of clinical microbiology.

[30]  H. Karch,et al.  Single primer pair for amplifying segments of distinct Shiga-like-toxin genes by polymerase chain reaction , 1989, Journal of clinical microbiology.

[31]  D. Smith,et al.  Evaluation of the Phadebact ETEC-LT test for the heat-labile enterotoxin of Escherichia coli. , 1989, Zentralblatt fur Bakteriologie : international journal of medical microbiology.

[32]  É. Carniel,et al.  The gene coding for the 190,000-dalton iron-regulated protein of Yersinia species is present only in the highly pathogenic strains , 1989, Infection and immunity.

[33]  D. M. Olive,et al.  Detection of enterotoxigenic Escherichia coli after polymerase chain reaction amplification with a thermostable DNA polymerase , 1989, Journal of clinical microbiology.

[34]  H. Mollaret,et al.  Purification, location, and immunological characterization of the iron-regulated high-molecular-weight proteins of the highly pathogenic yersiniae , 1989, Infection and immunity.

[35]  D. Maneval,et al.  Characterization of enteroadherent-aggregative Escherichia coli, a putative agent of diarrheal disease. , 1988, The Journal of infectious diseases.

[36]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[37]  Jürgen Heesemann,et al.  Chromosomal-encoded siderophores are required for mouse virulence of enteropathogenic Yersinia species , 1987 .

[38]  J. Neilands,et al.  Molecular mechanism of regulation of siderophore-mediated iron assimilation. , 1987, Microbiological reviews.

[39]  G. Cornelis,et al.  Yersinia enterocolitica, a primary model for bacterial invasiveness. , 1987, Reviews of infectious diseases.

[40]  D. Portnoy,et al.  Role of a plasmid in the pathogenicity of Yersinia species. , 1985, Current topics in microbiology and immunology.

[41]  J. Neilands,et al.  Siderophores of bacteria and fungi. , 1984, Microbiological sciences.

[42]  R. Calvert Gel electrophoresis of proteins: A practical approach , 1982 .

[43]  Larry K. Pickering,et al.  Infections of the Gastrointestinal Tract , 1980, Current Topics in Infectious Disease.

[44]  E. Southern Detection of specific sequences among DNA fragments separated by gel electrophoresis. , 1975, Journal of molecular biology.

[45]  P. Reeves,et al.  Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group B , 1975, Journal of Bacteriology.

[46]  K.,et al.  Genetics of resistance to colicins in Escherichia coli K-12: cross-resistance among colicins of group A , 1975, Journal of bacteriology.

[47]  U. Schibler,et al.  Changes in size and secondary structure of the ribosomal transcription unit during vertebrate evolution. , 1975, Journal of molecular biology.

[48]  D. Stibenz [Introduction to polyacrylamide gel electrophoresis]. , 1975, Acta histochemica. Supplementband.

[49]  P. Hu,et al.  Specificity, Induction, and Absorption of Pesticin , 1972, Journal of bacteriology.