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Volume 147, Issue 11

The elements of the locus of enterocyte effacement in human and wild mammal isolates of : evolution by assemblage or disruption? Free

Abstract

is an excellent model for studying the evolution of pathogenicity since within one species various genes can be found in pathogenic islands and plasmids causing a wide spectrum of virulence. A collection of 122 strains from different human and wild mammal hosts were analysed by PCR and Southern hybridization for the presence of a subset of the genes included in the LEE (locus of enterocyte effacement). In the PCR analysis, two markers ( and genes) were found together in more strains (254%) than either were found alone. The gene was less frequently found alone (82%) than was the gene (156%). Four regions of the LEE were analysed in a subsample of 25 strains using Southern hybridization. The four regions were all present (44%), all absent (12%) or present in different combinations (44%) in a given strain. The flanking regions of the LEE showed the highest rate of hybridization (in 72% of the strains). The results indicate that the LEE is a dynamic genetic entity, both the complete gene cluster and the individual genes. The genes that comprise this locus seem to be horizontally acquired (or lost) in an independent way and may control other functions in non-pathogenic lineages. In this way, horizontal transfer may allow the gradual stepwise construction of gene cassettes facilitating coordinate regulation and expression of novel functions.

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Keyword(s): A-E, attaching-effacing , EAEC, enteroaggregative E. coli , EHEC, enterohaemorrhagic E. coli , EIEC, enteroinvasive E. coli , enterobacteriacae , EPEC, enteropathogenic E. coli , ETEC, enterotoxigenic E. coli , horizontal transfer , LEE, locus of enterocyte effacement , PAI, pathogenic island , pathogenic islands , UPGMA, unweighted pair group method with arithmetic means , UTI, urinary tract E. coli and wild isolates
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2001-11-01
2024-04-26
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References

  1. Beltrametti, F., Kresse, A. U. & Guzmán, C. A. (1999). Transcriptional regulation of the esp genes of enterohaemorrhagic Escherichia coli. J Bacteriol 181, 3409-3418. [Google Scholar]
  2. Blattner, F. R., Plunkett, I. G., Bloch, C. A. & 14 other authors (1997). The complete genome sequence of Escherichia coli K-12. Science 277, 1453–1462.[CrossRef] [Google Scholar]
  3. Cravioto, A., Gross, R. J., Scotland, S. M. & Rowe, B. (1979). An adhesive factor found in strains of Escherichia coli belonging to the traditional infantile enteropathogenic serotypes. Curr Microbiol 3, 95-99.[CrossRef] [Google Scholar]
  4. de la Cruz, F. & Davies, J. (2000). Horizontal gene transfer and the origin of species: lessons from bacteria. Trends Microbiol 8, 128-133.[CrossRef] [Google Scholar]
  5. Donnenberg, M. S. & Kaper, J. B. (1992). Enteropathogenic Escherichia coli. Infect Immun 60, 3953-3961. [Google Scholar]
  6. Dykhuizen, D. E. & Green, L. (1991). Recombination in Escherichia coli and the definition of biological species. J Bacteriol 173, 7257-7268. [Google Scholar]
  7. Elliot, S. J., Wainwright, L. A., McDaniel, T. K., Jarvis, K. G., Deng, Y. K., Lai, L. C., MacNamara, B. P., Donnenberg, M. S. & Kaper, J. B. (1998). The complete sequence of the locus of enterocyte effacement (LEE) from enteropathogenic Escherichia coli E2348/69. Mol Microbiol 28, 1-4. [Google Scholar]
  8. Finlay, B. B. & Abe, A. (1998). Enteropathogenic Escherichia coli interactions with host cells. Jpn J Med Sci Biol 51, 91-100.[CrossRef] [Google Scholar]
  9. Finlay, B. B. & Falkow, S. (1997). Common themes in microbial pathogenicity revisited. Mol Biol Microbiol Rev 61, 136-169. [Google Scholar]
  10. Guttman, D. S. (1997). Recombination and clonality in natural populations of Escherichia coli. Trends Ecol Evol 12, 16-22. [Google Scholar]
  11. Hamburg, M. (1979).Basic Statistics: a Modern Approach 2nd edn. New York:Harcourt Brace Jovanovich.
  12. Hartland, E. L., Batchelor, M., Delahay, R. M., Hale, C., Matthews, S., Dougan, G., Knutton, S., Connerton, I. & Frankel, G. (1999). Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol Microbiol 32, 151-158.[CrossRef] [Google Scholar]
  13. Ismaili, A., McWhirter, E., Handelsman, M. Y. C., Brunton, J. L. & Sherman, P. M. (1998). Divergent signal transduction responses to infection with attaching and effacing Escherichia coli. Infect Immun 66, 1688-1696. [Google Scholar]
  14. Jarvis, K. G., Girón, J. A., Jerse, A. E., Mc Daniel, T. K., Donnenberg, M. S. & Kaper, J. B. (1995). Enteropathogenic Escherichia coli contains a putative type III secretion system necessary for the export of proteins involved in attaching and effacing lesion formation. Proc Natl Acad Sci USA 92, 7996-8000.[CrossRef] [Google Scholar]
  15. Jerse, A. E. & Kaper, J. B. (1991). The eae gene of enteropathogenic Escherichia coli encodes a 94-kilodalton membrane protein, the expression of which is influenced by the EAF plasmid. Infect Immun 59, 4302-4309. [Google Scholar]
  16. Jerse, A. E., Yu, J., Tall, B. D. & Kaper, J. B. (1990). A genetic locus of enteropathogenic Escherichia coli necessary for the production of attaching and effacing lesions on tissue culture cells.Proc Natl Acad Sci USA 87, 7839-7843.[CrossRef] [Google Scholar]
  17. Kaper, J. B. (1998). The locus of enterocyte effacement pathogenicity island of shiga toxin-producing Escherichia coli O157:H7 and other attaching and effacing E. coli. Jpn J Med Sci Biol 51, 101-107.[CrossRef] [Google Scholar]
  18. Kenny, B. & Finlay, B. B. (1995). Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc Natl Acad Sci USA 92, 7991-7995.[CrossRef] [Google Scholar]
  19. Kenny, B. & Finlay, B. B. (1997). Intimin dependent binding of enteropathogenic Escherichia coli to host cells triggers novel signaling events, including tyrosine phosphorylation of phospholipase C-1. Infect Immun 65, 2528-2536. [Google Scholar]
  20. Kenny, B., DeVinney, R., Stein, M., Reinscheid, D. J., Frey, E. A. & Finlay, B. B. (1997). Enteropathogenic Escherichia coli (EPEC) transfers its receptor for intimate adherence into mammalian cells. Cell 91, 511-520.[CrossRef] [Google Scholar]
  21. Lawrence, J. G. (1997). Selfish operons and speciation by gene transfer. Trends Microbiol 5, 355-359.[CrossRef] [Google Scholar]
  22. Lederberg, J. (1998). Emerging infection: an evolutionary perspective. Emerg Infect Dis 4, 366-371.[CrossRef] [Google Scholar]
  23. Li, W.-H. (1997). Molecular phylogenetics: methods. In Molecular Evolution, pp. 144–146. Sunderland, MA: Sinauer.
  24. McDaniel, T. K., Jarvis, K. G., Donnenberg, M. S. & Kaper, J. B. (1995). A genetic locus of enterocyte effacement conserved among diverse enterobacterial pathogens. Proc Natl Acad Sci USA 92, 1664-1668.[CrossRef] [Google Scholar]
  25. McGraw, E. A., Li, J., Selander, R. K. & Whittam, T. S. (1999). Molecular evolution and mosaic structure of α, β, and γ intimins of pathogenic Escherichia coli.Mol Biol Evol 16, 12-22.[CrossRef] [Google Scholar]
  26. Maynard-Smith, J. (1992). Analysing the mosaic structure of genes.J Mol Evol 34, 126-129. [Google Scholar]
  27. Nataro, J. P. & Kaper, J. B. (1998). Diarrheagenic Escherichia coli. Clin Microbiol Rev 11, 142-201. [Google Scholar]
  28. Ochman, H. & Selander, R. K. (1984). Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157, 690-693. [Google Scholar]
  29. Orskov, F. & Orskov, I. (1984). Serotyping of Escherichia coli. In Methods in Microbiology, vol. 14. Edited by T. Bergan. London: Academic Press.
  30. Paton, A. W., Manning, P. A., Woodrow, M. C. & Paton, J. C. (1998). Translocated intimin receptors (Tir) of Shiga-toxigenic Escherichia coli isolates belonging to serogroup O26, O111 and O157 react with sera from patients with hemolitic-uremic syndrome and exhibit marked sequence heterogeneity. Infect Immun 66, 5580-5586. [Google Scholar]
  31. Peek, A. S., Souza, V., Eguiarte, L. E. & Gaut, B. S. (2001). Selection and recombination at the type 1-fimbrial major subunit (fimA) in natural isolates of Escherichia coli. J Mol Evol 52, 193-204. [Google Scholar]
  32. Reeves, P. R. (1992). Variation in O-antigens, niche-specific selection and bacterial populations. FEMS Microbiol Lett 100, 509-516.[CrossRef] [Google Scholar]
  33. Reeves, P. R. (1993). Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale. Trends Genet 9, 17-22.[CrossRef] [Google Scholar]
  34. Reid, S. D., Herbelin, C. J., Bumbaugh, A. C., Selander, R. K. & Whittam, T. S. (2000). Parallel evolution of virulence in pathogenic Escherichia coli. Nature 406, 64-67.[CrossRef] [Google Scholar]
  35. Southern, E. M. (1975). Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98, 503.[CrossRef] [Google Scholar]
  36. Souza, V., Rocha, M., Valera, A. & Eguiarte, L. E. (1999). Genetic structure of natural populations of Escherichia coli in wild hosts on different continents. Appl Environ Microbiol 65, 3373-3385. [Google Scholar]
  37. Taylor, K. A., O’Connell, C. B., Luther, P. W. & Donnenberg, M. S. (1998). The espB protein of enteropathogenic Escherichia coli is targeted to the cytoplasm of infected HeLa cells. Infect Immun 66, 5501-5507. [Google Scholar]
  38. Tzipori, S., Gunzer, F., Donnenberg, M. S., de Montigny, L., Kaper, J. B. & Donohue-Rolfe, A. (1995). The role of eaeA gene in diarrhea and neurological complications in a gnotobiotic piglet model of enterohaemorrhagic Escherichia coli infection. Infect Immun 63, 3621-3627. [Google Scholar]
  39. Whittam, T. S. (1990). ETDIV and ETCLUS programs. Pennsylvania, PA: Pennsylvania State University.
  40. Wieler, L. H., McDaniel, T. K., Whittam, T. S. & Kaper, J. B. (1997). Insertion site of the locus of enterocyte effacement in enteropathogenic and enterohaemorrhagic Escherichia coli differs in relation to the clonal genealogy of the strains. FEMS Microbiol Lett 156, 49-53.[CrossRef] [Google Scholar]
  41. Zhao, S., Mitchell, S. E., Meng, J., Doyle, M. P. & Kresovich, S. (1995). Cloning and nucleotide sequence of a gene upstream of the eaeA gene of enterohaemorrhagic Escherichia coli O157:H7. FEMS Microbiol Lett 133, 35-39.[CrossRef] [Google Scholar]
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The elements of the locus of enterocyte effacement in human and wild mammal isolates of Escherichia coli: evolution by assemblage or disruption?
Microbiology 147, 3149 (2001); https://doi.org/10.1099/00221287-147-11-3149
/content/journal/micro/10.1099/00221287-147-11-3149
/content/journal/micro/10.1099/00221287-147-11-3149
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