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Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna

Background: The emergence of multidrug-resistant bacteria remains poorly understood in the wild ecosystem and at the interface of habitats. Here, we explored the spread of Escherichia coli containing IncI1-ST3 plasmid encoding resistance gene cefotaximase-Munich-1 (bla(CTX-M-1)) in human-influenced...

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Autores principales: Beyrouthy, Racha, Sabença, Carolina, Robin, Frédéric, Poeta, Patricia, Igrejas, Giberto, Bonnet, Richard
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8305760/
https://www.ncbi.nlm.nih.gov/pubmed/34361907
http://dx.doi.org/10.3390/microorganisms9071471
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author Beyrouthy, Racha
Sabença, Carolina
Robin, Frédéric
Poeta, Patricia
Igrejas, Giberto
Bonnet, Richard
author_facet Beyrouthy, Racha
Sabença, Carolina
Robin, Frédéric
Poeta, Patricia
Igrejas, Giberto
Bonnet, Richard
author_sort Beyrouthy, Racha
collection PubMed
description Background: The emergence of multidrug-resistant bacteria remains poorly understood in the wild ecosystem and at the interface of habitats. Here, we explored the spread of Escherichia coli containing IncI1-ST3 plasmid encoding resistance gene cefotaximase-Munich-1 (bla(CTX-M-1)) in human-influenced habitats and wild fauna using a genomic approach. Methods. Multilocus sequence typing (MLST), single-nucleotide polymorphism comparison, synteny-based analysis and data mining approaches were used to analyse a dataset of genomes and circularised plasmids. Results. CTX-M-1 E. coli sequence types (STs) were preferentially associated with ecosystems. Few STs were shared by distinct habitats. IncI1-ST3-bla(CTX-M-1) plasmids are disseminated among all E. coli phylogroups. The main divergences in plasmids were located in a shuffling zone including bla(CTX-M-1) inserted in a conserved site. This insertion hot spot exhibited diverse positions and orientations in a zone-modulating conjugation, and the resulting synteny was associated with geographic and biological sources. Conclusions. The ecological success of IncI1-ST3-bla(CTX-M-1) appears less linked to the spread of their bacterial recipients than to their ability to transfer in a broad spectrum of bacterial lineages. This feature is associated with the diversity of their shuffling conjugation region that contain bla(CTX-M-1). These might be involved in the resistance to antimicrobials, but also in their spread.
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spelling pubmed-83057602021-07-25 Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna Beyrouthy, Racha Sabença, Carolina Robin, Frédéric Poeta, Patricia Igrejas, Giberto Bonnet, Richard Microorganisms Article Background: The emergence of multidrug-resistant bacteria remains poorly understood in the wild ecosystem and at the interface of habitats. Here, we explored the spread of Escherichia coli containing IncI1-ST3 plasmid encoding resistance gene cefotaximase-Munich-1 (bla(CTX-M-1)) in human-influenced habitats and wild fauna using a genomic approach. Methods. Multilocus sequence typing (MLST), single-nucleotide polymorphism comparison, synteny-based analysis and data mining approaches were used to analyse a dataset of genomes and circularised plasmids. Results. CTX-M-1 E. coli sequence types (STs) were preferentially associated with ecosystems. Few STs were shared by distinct habitats. IncI1-ST3-bla(CTX-M-1) plasmids are disseminated among all E. coli phylogroups. The main divergences in plasmids were located in a shuffling zone including bla(CTX-M-1) inserted in a conserved site. This insertion hot spot exhibited diverse positions and orientations in a zone-modulating conjugation, and the resulting synteny was associated with geographic and biological sources. Conclusions. The ecological success of IncI1-ST3-bla(CTX-M-1) appears less linked to the spread of their bacterial recipients than to their ability to transfer in a broad spectrum of bacterial lineages. This feature is associated with the diversity of their shuffling conjugation region that contain bla(CTX-M-1). These might be involved in the resistance to antimicrobials, but also in their spread. MDPI 2021-07-09 /pmc/articles/PMC8305760/ /pubmed/34361907 http://dx.doi.org/10.3390/microorganisms9071471 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Beyrouthy, Racha
Sabença, Carolina
Robin, Frédéric
Poeta, Patricia
Igrejas, Giberto
Bonnet, Richard
Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title_full Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title_fullStr Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title_full_unstemmed Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title_short Successful Dissemination of Plasmid-Mediated Extended-Spectrum β-Lactamases in Enterobacterales over Humans to Wild Fauna
title_sort successful dissemination of plasmid-mediated extended-spectrum β-lactamases in enterobacterales over humans to wild fauna
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8305760/
https://www.ncbi.nlm.nih.gov/pubmed/34361907
http://dx.doi.org/10.3390/microorganisms9071471
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