Phylogenetic relationships among clonal groups of extraintestinal pathogenic Escherichia coli as assessed by multi-locus sequence analysis

James R. Johnson, Krista L. Owens, Connie R. Clabots, Scott J. Weissman, Steven B. Cannon

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65 Scopus citations

Abstract

The evolutionary origins of extraintestinal pathogenic Escherichia coli (ExPEC) remain uncertain despite these organisms' relevance to human disease. A valid understanding of ExPEC phylogeny is needed as a framework against which the observed distribution of virulence factors and clinical associations can be analyzed. Accordingly, phylogenetic relationships were defined by multi-locus sequence analysis among 44 representatives of selected ExPEC clonal groups and the E. coli Reference (ECOR) collection. Recombination, which significantly obscured the phylogenetic signal for several strains, was dealt with by excluding strains or specific sequences. Conflicting overall phylogenies, and internal phylogenies for virulence-associated phylogenetic group B2, were inferred depending on the specific dataset (i.e., how extensively purged of recombination), outgroup (Salmonella enterica and/or Escherichia fergusonii), and analysis method (neighbor joining, maximum parsimony, maximum likelihood, or Bayesian likelihood). Nonetheless, the major E. coli phylogenetic groups A, B1, and B2 were consistently well resolved, as was a major sub-component of group D and an ECOR 37-O157:H7 clade. Moreover, nine important ExPEC clonal groups within groups B2 and D, characterized by serotypes O6:K2:H1, O18:K1:H7, O6:H31, and O4:K+:H+ (from group B2), and O1:K1:H-, O7:K1:H-, O157:K+:H (non-7), O15:K52:H1, and O11/17/77:K52:H18 ("clonal group A") (from group D), were consistently well resolved, regardless of clinical background (cystitis, pyelonephritis, neonatal meningitis, sepsis, or fecal), host group, geographical origin, and virulence profile. Among the group B2-derived clonal groups the O6:K2:H1 clade appeared basal. Within group D, "clonal group A" and the O15:K52:H1 clonal group were consistently placed with ECOR 47 and ECOR 44, respectively, as nearest neighbors. These findings clarify phylogenetic relationships among key ExPEC clonal groups but also emphasize that recombination appears to obscure the oldest evolutionary relationships, despite extensive targeted sequencing and use of a wide range of analysis techniques.

Original languageEnglish (US)
Pages (from-to)1702-1713
Number of pages12
JournalMicrobes and Infection
Volume8
Issue number7
DOIs
StatePublished - Jun 2006

Bibliographical note

Funding Information:
This material is based upon work supported by Office of Research and Development, Medical Research Service, Department of Veterans Affairs, National Research Initiative (NRI) Competitive Grants Program/United States Department of Agriculture grant 00-35212-9408, and National Institutes of Health grant R01-GM060731 (all to J.R.J.). Andrew Baumgarten, Eric Brown, Anthony Dean, Daniel Dykhuizen, and Evgeni Sokurenko provided helpful suggestions regarding recombination and phylogenetic analysis. Thierry Wirth provided the primer sequences. Erick Denamur and Thomas Whittam provided supplemental multilocus sequence datasets. Dave Prentiss (VA Medical Center) prepared the figures. A tree based on fumC sequence from this study was shown in a prior publication (Johnson JR, Owens K, Manges A, Riley L, 2004. Rapid and specific detection of Escherichia coli Clonal Group A by gene-specific PCR. J Clin Microbiol 42:2618-22). Potential conflicts of interest: J.R.J. has received grant support and/or honoraria from Bayer, Wyeth-Ayerst, Ortho-McNeil, Merck, and Rochester Medical Group. The other authors have no potential financial conflicts of interest.

Copyright:
Copyright 2008 Elsevier B.V., All rights reserved.

Keywords

  • Antimicrobial drug resistance
  • Bayesian analysis
  • Clone cells
  • Cluster analysis
  • Cystitis
  • DNA sequence analysis
  • Escherichia coli infections
  • Evolution
  • Genetic recombination
  • Maximum likelihood estimates
  • Meningitis
  • Pathogenicity
  • Phylogeny
  • Pyelonephritis
  • Sepsis
  • Virulence factors

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