Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131

ABSTRACT The emergence of multidrug-resistant Escherichia coli ST131 is a major worldwide public health problem in humans. According to the “one health” approach, this study investigated animal reservoirs of ST131, their relationships with human strains, and the genetic features associated with host...

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Autores principales:	Richard Bonnet, Racha Beyrouthy, Marisa Haenni, Marie-Hélène Nicolas-Chanoine, Guillaume Dalmasso, Jean-Yves Madec
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2021
Materias:	ST131 Escherichia coli population structure extended-spectrum beta-lactamase antibiotic resistance virulence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2b78d2eb57e6472db896490e59c5537d
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spelling	oai:doaj.org-article:2b78d2eb57e6472db896490e59c5537d2021-11-10T18:37:51ZHost Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST13110.1128/mBio.01451-212150-7511https://doaj.org/article/2b78d2eb57e6472db896490e59c5537d2021-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01451-21https://doaj.org/toc/2150-7511ABSTRACT The emergence of multidrug-resistant Escherichia coli ST131 is a major worldwide public health problem in humans. According to the “one health” approach, this study investigated animal reservoirs of ST131, their relationships with human strains, and the genetic features associated with host colonization. High-quality genomes originating from human, avian, and canine hosts were classified on the basis of their accessory gene content using pangenomic. Pangenomic clusters and subclusters were specifically and significantly associated with hosts. The functions of clustering accessory genes were mainly enriched in functions involved in DNA acquisition, interactions, and virulence (e.g., pathogenesis, response to biotic stimulus and interaction between organisms). Accordingly, networks of cooccurrent host interaction factors were significantly associated with the pangenomic clusters and the originating hosts. The avian strains exhibited a specific content in virulence factors. Rarely found in humans, they corresponded to pathovars responsible for severe human infections. An emerging subcluster significantly associated with both human and canine hosts was evidenced. This ability to significantly colonize canine hosts in addition to humans was associated with a specific content in virulence factors (VFs) and metabolic functions encoded by a new pathogenicity island in ST131 and an improved fitness that is probably involved in its emergence. Overall, VF content, unlike the determinants of antimicrobial resistance, appeared as a key actor of bacterial host adaptation. The host dimension emerges as a major driver of genetic evolution that shapes ST131 genome, enhances its diversity, and favors its dissemination. IMPORTANCE Until now, there has been no indication that the evolutionary dynamics of Escherichia coli ST131 may reflect independent and host-specific adaptation of this lineage outside humans. In contrast, the limited number of ST131 reports in animals supported the common view that it rather reflects a spillover of the human sector. This study uncovered a link between host, ST131 population structure, and virulence factor content which appeared to reflect adaptation to hosts. This study helps to better understand the reservoir of ST131, the putative transmission flux, associated risks and the evolutionary dynamics of this bacterial population and highlights a paradigm in which host colonization stands as a key ecological force of the ST131 evolution.Richard BonnetRacha BeyrouthyMarisa HaenniMarie-Hélène Nicolas-ChanoineGuillaume DalmassoJean-Yves MadecAmerican Society for MicrobiologyarticleST131Escherichia colipopulation structureextended-spectrum beta-lactamaseantibiotic resistancevirulenceMicrobiologyQR1-502ENmBio, Vol 12, Iss 4 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	ST131 Escherichia coli population structure extended-spectrum beta-lactamase antibiotic resistance virulence Microbiology QR1-502
spellingShingle	ST131 Escherichia coli population structure extended-spectrum beta-lactamase antibiotic resistance virulence Microbiology QR1-502 Richard Bonnet Racha Beyrouthy Marisa Haenni Marie-Hélène Nicolas-Chanoine Guillaume Dalmasso Jean-Yves Madec Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
description	ABSTRACT The emergence of multidrug-resistant Escherichia coli ST131 is a major worldwide public health problem in humans. According to the “one health” approach, this study investigated animal reservoirs of ST131, their relationships with human strains, and the genetic features associated with host colonization. High-quality genomes originating from human, avian, and canine hosts were classified on the basis of their accessory gene content using pangenomic. Pangenomic clusters and subclusters were specifically and significantly associated with hosts. The functions of clustering accessory genes were mainly enriched in functions involved in DNA acquisition, interactions, and virulence (e.g., pathogenesis, response to biotic stimulus and interaction between organisms). Accordingly, networks of cooccurrent host interaction factors were significantly associated with the pangenomic clusters and the originating hosts. The avian strains exhibited a specific content in virulence factors. Rarely found in humans, they corresponded to pathovars responsible for severe human infections. An emerging subcluster significantly associated with both human and canine hosts was evidenced. This ability to significantly colonize canine hosts in addition to humans was associated with a specific content in virulence factors (VFs) and metabolic functions encoded by a new pathogenicity island in ST131 and an improved fitness that is probably involved in its emergence. Overall, VF content, unlike the determinants of antimicrobial resistance, appeared as a key actor of bacterial host adaptation. The host dimension emerges as a major driver of genetic evolution that shapes ST131 genome, enhances its diversity, and favors its dissemination. IMPORTANCE Until now, there has been no indication that the evolutionary dynamics of Escherichia coli ST131 may reflect independent and host-specific adaptation of this lineage outside humans. In contrast, the limited number of ST131 reports in animals supported the common view that it rather reflects a spillover of the human sector. This study uncovered a link between host, ST131 population structure, and virulence factor content which appeared to reflect adaptation to hosts. This study helps to better understand the reservoir of ST131, the putative transmission flux, associated risks and the evolutionary dynamics of this bacterial population and highlights a paradigm in which host colonization stands as a key ecological force of the ST131 evolution.
format	article
author	Richard Bonnet Racha Beyrouthy Marisa Haenni Marie-Hélène Nicolas-Chanoine Guillaume Dalmasso Jean-Yves Madec
author_facet	Richard Bonnet Racha Beyrouthy Marisa Haenni Marie-Hélène Nicolas-Chanoine Guillaume Dalmasso Jean-Yves Madec
author_sort	Richard Bonnet
title	Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
title_short	Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
title_full	Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
title_fullStr	Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
title_full_unstemmed	Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131
title_sort	host colonization as a major evolutionary force favoring the diversity and the emergence of the worldwide multidrug-resistant <italic toggle="yes">escherichia coli</italic> st131
publisher	American Society for Microbiology
publishDate	2021
url	https://doaj.org/article/2b78d2eb57e6472db896490e59c5537d
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Host Colonization as a Major Evolutionary Force Favoring the Diversity and the Emergence of the Worldwide Multidrug-Resistant <italic toggle="yes">Escherichia coli</italic> ST131

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