Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection

ABSTRACT The Escherichia coli lineage known as clonal complex 95 (CC95) is a cosmopolitan human-associated lineage responsible for a significant fraction of extraintestinal infections of humans. Whole-genome sequence data of 200 CC95 strains from various origins enabled determination of the CC95 pan...

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Autores principales: David M. Gordon, Sarah Geyik, Olivier Clermont, Claire L. O’Brien, Shiwei Huang, Charmalie Abayasekara, Ashwin Rajesh, Karina Kennedy, Peter Collignon, Paul Pavli, Christophe Rodriguez, Brian D. Johnston, James R. Johnson, Jean-Winoc Decousser, Erick Denamur
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:8f972b6a4f3540c5bfec7219b7a3e9902021-11-15T15:21:46ZFine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection10.1128/mSphere.00168-172379-5042https://doaj.org/article/8f972b6a4f3540c5bfec7219b7a3e9902017-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00168-17https://doaj.org/toc/2379-5042ABSTRACT The Escherichia coli lineage known as clonal complex 95 (CC95) is a cosmopolitan human-associated lineage responsible for a significant fraction of extraintestinal infections of humans. Whole-genome sequence data of 200 CC95 strains from various origins enabled determination of the CC95 pangenome. The pangenome analysis revealed that strains of the complex could be assigned to one of five subgroups that vary in their serotype, extraintestinal virulence, virulence gene content, and antibiotic resistance gene profile. A total of 511 CC95 strains isolated from humans living in France, Australia, and the United States were screened for their subgroup membership using a PCR-based method. The CC95 subgroups are nonrandomly distributed with respect to their geographic origin. The relative frequency of the subgroups was shown to change through time, although the nature of the changes varies with continent. Strains of the subgroups are also nonrandomly distributed with respect to source of isolation (blood, urine, or feces) and host sex. Collectively, the evidence indicates that although strains belonging to CC95 may be cosmopolitan, human movement patterns have been insufficient to homogenize the distribution of the CC95 subgroups. Rather, the manner in which CC95 strains evolve appears to vary both spatially and temporally. Although CC95 strains appeared globally as pandemic, fine-scale structure analysis shows epidemic patterns of the CC95 subgroups. Furthermore, the observation that the relative frequency of CC95 subgroups at a single locality has changed over time indicates that the relative fitness of the subgroups has changed. IMPORTANCE Escherichia coli clonal complex 95 represents a cosmopolitan, genetically diverse lineage, and the extensive substructure observed in this lineage is epidemiologically and clinically relevant. The frequency with which CC95 strains are responsible for extraintestinal infection appears to have been stable over the past 15 years. However, the different subgroups identified within this lineage have an epidemic structure depending on the host, sample, continent, and time. Thus, the evolution and spread of strains belonging to CC95 are very different from those of another cosmopolitan human-associated clonal complex, CC131, which has increased significantly in frequency as a cause of extraintestinal infection over the past 15 years due to the evolution and spread of two very closely related, nearly monomorphic lineages.David M. GordonSarah GeyikOlivier ClermontClaire L. O’BrienShiwei HuangCharmalie AbayasekaraAshwin RajeshKarina KennedyPeter CollignonPaul PavliChristophe RodriguezBrian D. JohnstonJames R. JohnsonJean-Winoc DecousserErick DenamurAmerican Society for Microbiologyarticleclonal complex 95Escherichia coliepidemiologypopulation geneticsMicrobiologyQR1-502ENmSphere, Vol 2, Iss 3 (2017)
institution DOAJ
collection DOAJ
language EN
topic clonal complex 95
Escherichia coli
epidemiology
population genetics
Microbiology
QR1-502
spellingShingle clonal complex 95
Escherichia coli
epidemiology
population genetics
Microbiology
QR1-502
David M. Gordon
Sarah Geyik
Olivier Clermont
Claire L. O’Brien
Shiwei Huang
Charmalie Abayasekara
Ashwin Rajesh
Karina Kennedy
Peter Collignon
Paul Pavli
Christophe Rodriguez
Brian D. Johnston
James R. Johnson
Jean-Winoc Decousser
Erick Denamur
Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
description ABSTRACT The Escherichia coli lineage known as clonal complex 95 (CC95) is a cosmopolitan human-associated lineage responsible for a significant fraction of extraintestinal infections of humans. Whole-genome sequence data of 200 CC95 strains from various origins enabled determination of the CC95 pangenome. The pangenome analysis revealed that strains of the complex could be assigned to one of five subgroups that vary in their serotype, extraintestinal virulence, virulence gene content, and antibiotic resistance gene profile. A total of 511 CC95 strains isolated from humans living in France, Australia, and the United States were screened for their subgroup membership using a PCR-based method. The CC95 subgroups are nonrandomly distributed with respect to their geographic origin. The relative frequency of the subgroups was shown to change through time, although the nature of the changes varies with continent. Strains of the subgroups are also nonrandomly distributed with respect to source of isolation (blood, urine, or feces) and host sex. Collectively, the evidence indicates that although strains belonging to CC95 may be cosmopolitan, human movement patterns have been insufficient to homogenize the distribution of the CC95 subgroups. Rather, the manner in which CC95 strains evolve appears to vary both spatially and temporally. Although CC95 strains appeared globally as pandemic, fine-scale structure analysis shows epidemic patterns of the CC95 subgroups. Furthermore, the observation that the relative frequency of CC95 subgroups at a single locality has changed over time indicates that the relative fitness of the subgroups has changed. IMPORTANCE Escherichia coli clonal complex 95 represents a cosmopolitan, genetically diverse lineage, and the extensive substructure observed in this lineage is epidemiologically and clinically relevant. The frequency with which CC95 strains are responsible for extraintestinal infection appears to have been stable over the past 15 years. However, the different subgroups identified within this lineage have an epidemic structure depending on the host, sample, continent, and time. Thus, the evolution and spread of strains belonging to CC95 are very different from those of another cosmopolitan human-associated clonal complex, CC131, which has increased significantly in frequency as a cause of extraintestinal infection over the past 15 years due to the evolution and spread of two very closely related, nearly monomorphic lineages.
format article
author David M. Gordon
Sarah Geyik
Olivier Clermont
Claire L. O’Brien
Shiwei Huang
Charmalie Abayasekara
Ashwin Rajesh
Karina Kennedy
Peter Collignon
Paul Pavli
Christophe Rodriguez
Brian D. Johnston
James R. Johnson
Jean-Winoc Decousser
Erick Denamur
author_facet David M. Gordon
Sarah Geyik
Olivier Clermont
Claire L. O’Brien
Shiwei Huang
Charmalie Abayasekara
Ashwin Rajesh
Karina Kennedy
Peter Collignon
Paul Pavli
Christophe Rodriguez
Brian D. Johnston
James R. Johnson
Jean-Winoc Decousser
Erick Denamur
author_sort David M. Gordon
title Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
title_short Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
title_full Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
title_fullStr Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
title_full_unstemmed Fine-Scale Structure Analysis Shows Epidemic Patterns of Clonal Complex 95, a Cosmopolitan <named-content content-type="genus-species">Escherichia coli</named-content> Lineage Responsible for Extraintestinal Infection
title_sort fine-scale structure analysis shows epidemic patterns of clonal complex 95, a cosmopolitan <named-content content-type="genus-species">escherichia coli</named-content> lineage responsible for extraintestinal infection
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/8f972b6a4f3540c5bfec7219b7a3e990
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