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Research Article

Global dissemination of a multidrug resistant Escherichia coli clone

Nicola K. Petty, Nouri L. Ben Zakour, Mitchell Stanton-Cook, Elizabeth Skippington, Makrina Totsika, Brian M. Forde, Minh-Duy Phan, Danilo Gomes Moriel, Kate M. Peters, Mark Davies, Benjamin A. Rogers, Gordon Dougan, Jesús Rodriguez-Baño, Alvaro Pascual, Johann D. D. Pitout, Mathew Upton, David L. Paterson, Timothy R. Walsh, Mark A. Schembri, and Scott A. Beatson
  1. aAustralian Infectious Diseases Research Centre, and
  2. bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
  3. cThe ithree institute, University of Technology Sydney, Sydney, NSW 2007, Australia;
  4. dWellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
  5. eUniversity of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital Campus, The University of Queensland, Brisbane, QLD 4029, Australia;
  6. fUnidad Clínica de Enfermedades Infecciosas y Microbiología, Hospital Universitario Virgen Macarena, 41007 Seville, Spain;
  7. gDepartmentos de Medicina y Microbiología, Universidad de Sevilla, 41009 Seville, Spain;
  8. hDivision of Microbiology, Calgary Laboratory Services, Calgary, AB, Canada T2L 2KB;
  9. iDepartment of Pathology and Laboratory Medicine, and Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, AB, Canada T2N 1N4;
  10. jSchool of Biomedical and Healthcare Sciences, Plymouth University, Plymouth PL4 8AA, United Kingdom;
  11. kSchool of Medicine, Cardiff University, Cardiff CF14 4XN, United Kingdom

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PNAS first published March 31, 2014; https://doi.org/10.1073/pnas.1322678111
Nicola K. Petty
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
cThe ithree institute, University of Technology Sydney, Sydney, NSW 2007, Australia;
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Nouri L. Ben Zakour
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Mitchell Stanton-Cook
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Elizabeth Skippington
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Makrina Totsika
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Brian M. Forde
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Minh-Duy Phan
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Danilo Gomes Moriel
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Kate M. Peters
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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Mark Davies
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
dWellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
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Benjamin A. Rogers
eUniversity of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital Campus, The University of Queensland, Brisbane, QLD 4029, Australia;
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Gordon Dougan
dWellcome Trust Sanger Institute, Hinxton, Cambridge CB10 1SA, United Kingdom;
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Jesús Rodriguez-Baño
fUnidad Clínica de Enfermedades Infecciosas y Microbiología, Hospital Universitario Virgen Macarena, 41007 Seville, Spain;
gDepartmentos de Medicina y Microbiología, Universidad de Sevilla, 41009 Seville, Spain;
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Alvaro Pascual
fUnidad Clínica de Enfermedades Infecciosas y Microbiología, Hospital Universitario Virgen Macarena, 41007 Seville, Spain;
gDepartmentos de Medicina y Microbiología, Universidad de Sevilla, 41009 Seville, Spain;
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Johann D. D. Pitout
hDivision of Microbiology, Calgary Laboratory Services, Calgary, AB, Canada T2L 2KB;
iDepartment of Pathology and Laboratory Medicine, and Department of Microbiology and Infectious Diseases, University of Calgary, Calgary, AB, Canada T2N 1N4;
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Mathew Upton
jSchool of Biomedical and Healthcare Sciences, Plymouth University, Plymouth PL4 8AA, United Kingdom;
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David L. Paterson
aAustralian Infectious Diseases Research Centre, and
eUniversity of Queensland Centre for Clinical Research, Royal Brisbane and Women's Hospital Campus, The University of Queensland, Brisbane, QLD 4029, Australia;
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Timothy R. Walsh
kSchool of Medicine, Cardiff University, Cardiff CF14 4XN, United Kingdom
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Mark A. Schembri
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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  • For correspondence: s.beatson@uq.edu.au m.schembri@uq.edu.au
Scott A. Beatson
aAustralian Infectious Diseases Research Centre, and
bSchool of Chemistry and Molecular Biosciences, The University of Queensland, Brisbane, QLD 4072, Australia;
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  • For correspondence: s.beatson@uq.edu.au m.schembri@uq.edu.au
  1. Edited by Scott J. Hultgren, Washington University School of Medicine, St. Louis, MO, and approved March 4, 2014 (received for review December 5, 2013)

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Significance

Escherichia coli sequence type 131 (ST131) is a globally disseminated multidrug-resistant clone associated with human urinary tract and bloodstream infections. Here, we have used genome sequencing to map the temporal and spatial relationship of a large collection of E. coli ST131 strains isolated from six distinct geographical regions across the world. We show that E. coli ST131 strains are distinct from other extraintestinal pathogenic E. coli and arose from a single progenitor strain prior to the year 2000.

Abstract

Escherichia coli sequence type 131 (ST131) is a globally disseminated, multidrug resistant (MDR) clone responsible for a high proportion of urinary tract and bloodstream infections. The rapid emergence and successful spread of E. coli ST131 is strongly associated with several factors, including resistance to fluoroquinolones, high virulence gene content, the possession of the type 1 fimbriae FimH30 allele, and the production of the CTX-M-15 extended spectrum β-lactamase (ESBL). Here, we used genome sequencing to examine the molecular epidemiology of a collection of E. coli ST131 strains isolated from six distinct geographical locations across the world spanning 2000–2011. The global phylogeny of E. coli ST131, determined from whole-genome sequence data, revealed a single lineage of E. coli ST131 distinct from other extraintestinal E. coli strains within the B2 phylogroup. Three closely related E. coli ST131 sublineages were identified, with little association to geographic origin. The majority of single-nucleotide variants associated with each of the sublineages were due to recombination in regions adjacent to mobile genetic elements (MGEs). The most prevalent sublineage of ST131 strains was characterized by fluoroquinolone resistance, and a distinct virulence factor and MGE profile. Four different variants of the CTX-M ESBL–resistance gene were identified in our ST131 strains, with acquisition of CTX-M-15 representing a defining feature of a discrete but geographically dispersed ST131 sublineage. This study confirms the global dispersal of a single E. coli ST131 clone and demonstrates the role of MGEs and recombination in the evolution of this important MDR pathogen.

  • bacterial evolution
  • genomics
  • phylogeography
  • genomic epidemiology

Footnotes

  • ↵1N.K.P. and N.L.B.Z. contributed equally to this work.

  • ↵2To whom correspondence may be addressed. E-mail: s.beatson{at}uq.edu.au or m.schembri{at}uq.edu.au.
  • Author contributions: N.K.P., N.L.B.Z., M.A.S., and S.A.B. designed research; N.K.P., N.L.B.Z., M.S.-C., E.S., M.T., B.M.F., M.-D.P., D.G.M., K.M.P., M.D., M.U., and S.A.B. performed research; M.S.-C., E.S., B.A.R., G.D., J.R.-B., A.P., J.D.D.P., M.U., D.L.P., and T.R.W. contributed new reagents/analytic tools; N.K.P., N.L.B.Z., M.A.S., and S.A.B. analyzed data; and N.K.P., N.L.B.Z., M.A.S., and S.A.B. wrote the paper.

  • The authors declare no conflict of interest.

  • This article is a PNAS Direct Submission.

  • Database deposition: The sequences reported in this paper have been deposited in the European Nucleotide Archive under study nos. ERP001354 and ERP004358. For a list of accession numbers, see Dataset S1.

  • This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1322678111/-/DCSupplemental.

Freely available online through the PNAS open access option.

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Global dissemination of E. coli ST131
Nicola K. Petty, Nouri L. Ben Zakour, Mitchell Stanton-Cook, Elizabeth Skippington, Makrina Totsika, Brian M. Forde, Minh-Duy Phan, Danilo Gomes Moriel, Kate M. Peters, Mark Davies, Benjamin A. Rogers, Gordon Dougan, Jesús Rodriguez-Baño, Alvaro Pascual, Johann D. D. Pitout, Mathew Upton, David L. Paterson, Timothy R. Walsh, Mark A. Schembri, Scott A. Beatson
Proceedings of the National Academy of Sciences Mar 2014, 201322678; DOI: 10.1073/pnas.1322678111

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Global dissemination of E. coli ST131
Nicola K. Petty, Nouri L. Ben Zakour, Mitchell Stanton-Cook, Elizabeth Skippington, Makrina Totsika, Brian M. Forde, Minh-Duy Phan, Danilo Gomes Moriel, Kate M. Peters, Mark Davies, Benjamin A. Rogers, Gordon Dougan, Jesús Rodriguez-Baño, Alvaro Pascual, Johann D. D. Pitout, Mathew Upton, David L. Paterson, Timothy R. Walsh, Mark A. Schembri, Scott A. Beatson
Proceedings of the National Academy of Sciences Mar 2014, 201322678; DOI: 10.1073/pnas.1322678111
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