Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains

ABSTRACT Enterococcus faecium, natively a gut commensal organism, emerged as a leading cause of multidrug-resistant hospital-acquired infection in the 1980s. As the living record of its adaptation to changes in habitat, we sequenced the genomes of 51 strains, isolated from various ecological environ...

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Autores principales:	François Lebreton, Willem van Schaik, Abigail Manson McGuire, Paul Godfrey, Allison Griggs, Varun Mazumdar, Jukka Corander, Lu Cheng, Sakina Saif, Sarah Young, Qiandong Zeng, Jennifer Wortman, Bruce Birren, Rob J. L. Willems, Ashlee M. Earl, Michael S. Gilmore
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/f679147b67f94fe797ff7b54ab909f2f
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spelling	oai:doaj.org-article:f679147b67f94fe797ff7b54ab909f2f2021-11-15T15:43:08ZEmergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains10.1128/mBio.00534-132150-7511https://doaj.org/article/f679147b67f94fe797ff7b54ab909f2f2013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00534-13https://doaj.org/toc/2150-7511ABSTRACT Enterococcus faecium, natively a gut commensal organism, emerged as a leading cause of multidrug-resistant hospital-acquired infection in the 1980s. As the living record of its adaptation to changes in habitat, we sequenced the genomes of 51 strains, isolated from various ecological environments, to understand how E. faecium emerged as a leading hospital pathogen. Because of the scale and diversity of the sampled strains, we were able to resolve the lineage responsible for epidemic, multidrug-resistant human infection from other strains and to measure the evolutionary distances between groups. We found that the epidemic hospital-adapted lineage is rapidly evolving and emerged approximately 75 years ago, concomitant with the introduction of antibiotics, from a population that included the majority of animal strains, and not from human commensal lines. We further found that the lineage that included most strains of animal origin diverged from the main human commensal line approximately 3,000 years ago, a time that corresponds to increasing urbanization of humans, development of hygienic practices, and domestication of animals, which we speculate contributed to their ecological separation. Each bifurcation was accompanied by the acquisition of new metabolic capabilities and colonization traits on mobile elements and the loss of function and genome remodeling associated with mobile element insertion and movement. As a result, diversity within the species, in terms of sequence divergence as well as gene content, spans a range usually associated with speciation. IMPORTANCE Enterococci, in particular vancomycin-resistant Enterococcus faecium, recently emerged as a leading cause of hospital-acquired infection worldwide. In this study, we examined genome sequence data to understand the bacterial adaptations that accompanied this transformation from microbes that existed for eons as members of host microbiota. We observed changes in the genomes that paralleled changes in human behavior. An initial bifurcation within the species appears to have occurred at a time that corresponds to the urbanization of humans and domestication of animals, and a more recent bifurcation parallels the introduction of antibiotics in medicine and agriculture. In response to the opportunity to fill niches associated with changes in human activity, a rapidly evolving lineage emerged, a lineage responsible for the vast majority of multidrug-resistant E. faecium infections.François LebretonWillem van SchaikAbigail Manson McGuirePaul GodfreyAllison GriggsVarun MazumdarJukka CoranderLu ChengSakina SaifSarah YoungQiandong ZengJennifer WortmanBruce BirrenRob J. L. WillemsAshlee M. EarlMichael S. GilmoreAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 François Lebreton Willem van Schaik Abigail Manson McGuire Paul Godfrey Allison Griggs Varun Mazumdar Jukka Corander Lu Cheng Sakina Saif Sarah Young Qiandong Zeng Jennifer Wortman Bruce Birren Rob J. L. Willems Ashlee M. Earl Michael S. Gilmore Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
description	ABSTRACT Enterococcus faecium, natively a gut commensal organism, emerged as a leading cause of multidrug-resistant hospital-acquired infection in the 1980s. As the living record of its adaptation to changes in habitat, we sequenced the genomes of 51 strains, isolated from various ecological environments, to understand how E. faecium emerged as a leading hospital pathogen. Because of the scale and diversity of the sampled strains, we were able to resolve the lineage responsible for epidemic, multidrug-resistant human infection from other strains and to measure the evolutionary distances between groups. We found that the epidemic hospital-adapted lineage is rapidly evolving and emerged approximately 75 years ago, concomitant with the introduction of antibiotics, from a population that included the majority of animal strains, and not from human commensal lines. We further found that the lineage that included most strains of animal origin diverged from the main human commensal line approximately 3,000 years ago, a time that corresponds to increasing urbanization of humans, development of hygienic practices, and domestication of animals, which we speculate contributed to their ecological separation. Each bifurcation was accompanied by the acquisition of new metabolic capabilities and colonization traits on mobile elements and the loss of function and genome remodeling associated with mobile element insertion and movement. As a result, diversity within the species, in terms of sequence divergence as well as gene content, spans a range usually associated with speciation. IMPORTANCE Enterococci, in particular vancomycin-resistant Enterococcus faecium, recently emerged as a leading cause of hospital-acquired infection worldwide. In this study, we examined genome sequence data to understand the bacterial adaptations that accompanied this transformation from microbes that existed for eons as members of host microbiota. We observed changes in the genomes that paralleled changes in human behavior. An initial bifurcation within the species appears to have occurred at a time that corresponds to the urbanization of humans and domestication of animals, and a more recent bifurcation parallels the introduction of antibiotics in medicine and agriculture. In response to the opportunity to fill niches associated with changes in human activity, a rapidly evolving lineage emerged, a lineage responsible for the vast majority of multidrug-resistant E. faecium infections.
format	article
author	François Lebreton Willem van Schaik Abigail Manson McGuire Paul Godfrey Allison Griggs Varun Mazumdar Jukka Corander Lu Cheng Sakina Saif Sarah Young Qiandong Zeng Jennifer Wortman Bruce Birren Rob J. L. Willems Ashlee M. Earl Michael S. Gilmore
author_facet	François Lebreton Willem van Schaik Abigail Manson McGuire Paul Godfrey Allison Griggs Varun Mazumdar Jukka Corander Lu Cheng Sakina Saif Sarah Young Qiandong Zeng Jennifer Wortman Bruce Birren Rob J. L. Willems Ashlee M. Earl Michael S. Gilmore
author_sort	François Lebreton
title	Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
title_short	Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
title_full	Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
title_fullStr	Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
title_full_unstemmed	Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains
title_sort	emergence of epidemic multidrug-resistant <named-content content-type="genus-species">enterococcus faecium</named-content> from animal and commensal strains
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/f679147b67f94fe797ff7b54ab909f2f
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Emergence of Epidemic Multidrug-Resistant <named-content content-type="genus-species">Enterococcus faecium</named-content> from Animal and Commensal Strains

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