1887

Abstract

Phosphoprotein phosphatases encoded by the and genes function in signal transduction pathways for degradation of misfolded proteins in the extracytoplasmic compartments of . In order to trace the evolution of genes and assess their roles in other enteric pathogens, the structure and distribution of these genes among closely related Shigella subgroups were studied. PCR amplification, probe hybridization studies and DNA sequencing were used to determine the genotypes of 58 strains from the four Shigella subgroups, Dysenteriae, Boydii, Sonnei and Flexneri. It was found that the alleles among Shigella subgroups were extremely susceptible to gene inactivation and that the mutations involved in allele inactivation were varied. They included IS insertions, gene replacement by an IS element, a small deletion within the gene or large deletion engulfing the entire gene region, and base substitutions that generated premature termination codons. As a result, of 58 strains studied, only eight (14 %) possessed intact and genes. Of the Shigella strains examined, 76 % (44/58) showed at least one of the alleles inactivated by one or more IS elements, including IS, IS, IS and IS. Phylogenetic analysis revealed that IS elements have been independently acquired in multiple lineages of Shigella, suggesting that loss of functional alleles has been advantageous during Shigella strain evolution.

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2005-08-01
2024-04-25
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References

  1. Blattner F. R., Plunkett G. 3rd, Bloch, C. A. 14 other authors 1997; The complete genome sequence of Escherichia coli K-12. Science 277:1453–1474 [CrossRef]
    [Google Scholar]
  2. Boyd E. F., Nelson K., Wang F. S., Whittam T. S., Selander R. K. 1994; Molecular genetic basis of allelic polymorphism in malate dehydrogenase ( mdh ) in natural populations of Escherichia coli and Salmonella enterica . Proc Natl Acad Sci U S A 91:1280–1284 [CrossRef]
    [Google Scholar]
  3. Brown E. W., LeClerc J. E., Li B., Payne W. L., Cebula T. A. 2001; Phylogenetic evidence for horizontal transfer of mutS alleles among naturally occurring Escherichia coli strains. J Bacteriol 183:1631–1644 [CrossRef]
    [Google Scholar]
  4. Brown E. W., Kotewicz M. L., Cebula T. A. 2002; Detection of recombination among Salmonella enterica strains using the incongruence length difference test. Mol Phylogenet Evol 24:102–120 [CrossRef]
    [Google Scholar]
  5. Cebula T. A. 1995; Allele-specific polymerase chain reaction (PCR) in mutation analysis: the Salmonella typhimurium his paradigm. In Application of Molecular Biology in Environmental Chemistry pp 11–33 Edited by Minear R. A., Ford A. M., Needham L. L., Karch N. J. Boca Raton, FL: CRC Press;
    [Google Scholar]
  6. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395 [CrossRef]
    [Google Scholar]
  7. DuPont H. L., Levine M. M., Hornick R. B., Formal S. B. 1989; Inoculum size in shigellosis and implications for expected mode of transmission. J Infect Dis 159:1126–1128 [CrossRef]
    [Google Scholar]
  8. Escobar-Paramo P., Giudicelli C., Parsot C., Denamur E. 2003; The evolutionary history of Shigella and enteroinvasive Escherichia coli revised. J Mol Evol 57:140–148 [CrossRef]
    [Google Scholar]
  9. Ewing W. H. 1949; Shigella nomenclature. J Bacteriol 57:633–638
    [Google Scholar]
  10. Farris J. S. 1983; The logical basis of phylogenetic analysis. In Procedings of the 2nd Meeting of the Willi Hennig Society Adv Cladistics 2 pp 7–36 Edited by Platnick N., Funk V. New York: Columbia University Press;
    [Google Scholar]
  11. Farris J. S., Kallersjo M., Kluge A. G., Bult C. 1995; Testing significance of incongruence. Cladistics 10:783–791
    [Google Scholar]
  12. Felsenstein J. 1985; Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39:783–791 [CrossRef]
    [Google Scholar]
  13. Forey P. L., Humphries C. J., Kitching I. L., Scotland R. W., Siebert D. J., Williams D. M. 1992 Cladistics: a Practical Course in Systematics Oxford: Clarendon Press;
    [Google Scholar]
  14. Herzer P. J., Inouye S., Inouye M., Whittam T. S. 1990; Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli . J Bacteriol 172:6175–6181
    [Google Scholar]
  15. Hyma K. E., Lacher D. W., Nelson A. M., Bumbaugh A. C., Janda J. M., Strockbine N. A., Young V. B., Whittam T. S. 2005; Evolutionary genetics of a new pathogenic Escherichia species: Escherichia albertii and related Shigella boydii strains. J Bacteriol 187:619–628 [CrossRef]
    [Google Scholar]
  16. Jin Q., Yuan Z., Xu J. & 30 other authors; 2002; Genome sequence of Shigella flexneri 2a: insights into pathogenicity through comparison with genomes of Escherichia coli K-12 and O157. Nucleic Acids Res 30:4432–4441 [CrossRef]
    [Google Scholar]
  17. Kotloff K. L., Winickff J. P., Ivanoff B., Clemens J. D., Swerdlow D. L., Sansonetti P. J., Adak G. K., Levine M. M. 1999; Global burden of Shigella infections: implications for vaccine development and implantation of control strategies. Bull WHO 77:651–666
    [Google Scholar]
  18. Lan R., Reeves P. 2002; Escherichia coli in disguise: molecular origins of Shigella . Microb Infect 4:1125–1132 [CrossRef]
    [Google Scholar]
  19. LeClerc J. E., Li B., Payne W. L., Cebula T. A. 1999; Promiscuous origin of a chimeric sequence in the Escherichia coli O157 : H7 genome. J Bacteriol 181:7614–7617
    [Google Scholar]
  20. Lecointre G., Rachdi L., Darlu P., Denamur E. 1998; Escherichia coli molecular phylogeny using the incongruence length difference test. Mol Biol Evol 15:1685–1695 [CrossRef]
    [Google Scholar]
  21. Li B., Tsui H.-C. T., LeClerc J. E., Dey M., Winkler M. E., Cebula T. A. 2003; Molecular analysis of mutS expression and mutation in natural isolates of pathogenic Escherichia coli . Microbiology 149:1323–1331 [CrossRef]
    [Google Scholar]
  22. Lin J., Lee I. S., Slonczewski J. L., Foster J. W. 1995; Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri , and Escherichia coli . J Bacteriol 177:4097–4104
    [Google Scholar]
  23. Missiakas D., Raina S. 1997; Signal transduction pathways in response to protein misfolding in the extracytoplasmic compartments of E. coli : role of two new phosphoprotein phosphatase PrpA and PrpB. EMBO J 16:1670–1685 [CrossRef]
    [Google Scholar]
  24. Maurelli A. T., Fernandez R. E., Bloch C. A., Rode C. K., Fasano A. 1998; “Black holes” and bacterial pathogenicity: a large genomic deletion that enhances the virulence of Shigella spp. and enteroinvasive Escherichia coli . Proc Natl Acad Sci U S A 95:3943–3948 [CrossRef]
    [Google Scholar]
  25. Nyman K., Nakamura K., Ohtsubo H., Ohtsubo E. 1981; Distribution of the insertion sequence IS 1 in gram-negative bacteria. Nature 289:609–612 [CrossRef]
    [Google Scholar]
  26. Ochman H., Selander R. K. 1984; Standard reference strains of Escherichia coli from natural populations. J Bacteriol 157:690–693
    [Google Scholar]
  27. Perna, N. T., Plunkett, G. 3rd, Burland V. 24 other authors 2001; Genome sequence of enterohaemorrhagic Escherichia coli O157 : H7. Nature 409:529–533 [CrossRef]
    [Google Scholar]
  28. Pupo G. M., Karaolis D. K. R., Lan R., Reeves P. R. 1997; Evolutionary relationships among pathogenic and nonpathogenic Escherichia coli strains inferred from mutilocus enzyme electrophoresis and mdh sequences studies. Infect Immun 65:2685–2692
    [Google Scholar]
  29. Pupo G. M., Lan R., Reeves P. R. 2000; Multiple independent origins of Shigella clones of Escherichia coli and convergent evolution of many of their characteristics. Proc Natl Acad Sci U S A 97:10567–10572 [CrossRef]
    [Google Scholar]
  30. Rezwan F., Lan R., Reeves P. R. 2004; Molecular basis of the indole-negative reaction in Shigella strains: extensive damages to the tna operon by insertion sequences. J Bacteriol 186:7460–7465 [CrossRef]
    [Google Scholar]
  31. Sagripanti J. L., Eklund C. A., Trost P. A., Jinneman K. C., Abeyta C. Jr, Kaysner C. A., Hill W. E. 1997; Comparative sensitivity of 13 species of pathogenic bacteria to seven chemical germicides. Am J Infect Control 25:335–339 [CrossRef]
    [Google Scholar]
  32. Schneider D., Duperchy E., Coursange E., Lenski R. E., Blot M. 2000; Long-term experimental evolution in Escherichia coli . IX. Characterization of insertion sequence-mediated mutation and rearrangements. Genetics 156:477–488
    [Google Scholar]
  33. Streisinger G., Okada Y., Emrich J., Newton J., Tsugita A., Terzaghi E., Inouye M. 1966; Frameshift mutations and the genetic code. Cold Spring Harbor Symp Quant Biol 31:77–84 [CrossRef]
    [Google Scholar]
  34. Swofford D. L. 1999 Phylogenetic analysis using parsimony (paup* v. 4.03b) program and documentation Washington, DC: Smithsonian Institution;
    [Google Scholar]
  35. Taormina P. J., Niemira B. A., Beuchat L. R. 2001; Inhibitory activity of honey against foodborne pathogens as influenced by the presence of hydrogen peroxide and level of antioxidant power. Int J Food Microbiol 69:217–225 [CrossRef]
    [Google Scholar]
  36. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal x Windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  37. Watarai M., Tobe T., Yashikawa M., Sasakawa C. 1995; Contact of Shigella with host cells triggers release of Ipa invasins and is an essential function of invasiveness. EMBO J 14:2461–2470
    [Google Scholar]
  38. Wei J., Goldberg M. B., Burland V. 14 other authors 2003; Complete genome sequence and comparative genomics of Shigella flexneri 2a strain 2457T. Infect Immun 71:2775–2786 [CrossRef]
    [Google Scholar]
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