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Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli
Plasmid-mediated antimicrobial resistance is a major contributor to the spread of resistance genes within bacterial communities. Successful plasmid spread depends upon a balance between plasmid fitness effects on the host and rates of horizontal transmission. While these key parameters are readily q...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
The Royal Society
2021
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8564601/ https://www.ncbi.nlm.nih.gov/pubmed/34727719 http://dx.doi.org/10.1098/rspb.2021.2027 |
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author | Duxbury, Sarah J. N. Alderliesten, Jesse B. Zwart, Mark P. Stegeman, Arjan Fischer, Egil A. J. de Visser, J. Arjan G. M. |
author_facet | Duxbury, Sarah J. N. Alderliesten, Jesse B. Zwart, Mark P. Stegeman, Arjan Fischer, Egil A. J. de Visser, J. Arjan G. M. |
author_sort | Duxbury, Sarah J. N. |
collection | PubMed |
description | Plasmid-mediated antimicrobial resistance is a major contributor to the spread of resistance genes within bacterial communities. Successful plasmid spread depends upon a balance between plasmid fitness effects on the host and rates of horizontal transmission. While these key parameters are readily quantified in vitro, the influence of interactions with other microbiome members is largely unknown. Here, we investigated the influence of three genera of lactic acid bacteria (LAB) derived from the chicken gastrointestinal microbiome on the spread of an epidemic narrow-range ESBL resistance plasmid, IncI1 carrying bla(CTX-M-1), in mixed cultures of isogenic Escherichia coli strains. Secreted products of LAB decreased E. coli growth rates in a genus-specific manner but did not affect plasmid transfer rates. Importantly, we quantified plasmid transfer rates by controlling for density-dependent mating opportunities. Parametrization of a mathematical model with our in vitro estimates illustrated that small fitness costs of plasmid carriage may tip the balance towards plasmid loss under growth conditions in the gastrointestinal tract. This work shows that microbial interactions can influence plasmid success and provides an experimental-theoretical framework for further study of plasmid transfer in a microbiome context. |
format | Online Article Text |
id | pubmed-8564601 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2021 |
publisher | The Royal Society |
record_format | MEDLINE/PubMed |
spelling | pubmed-85646012021-11-20 Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli Duxbury, Sarah J. N. Alderliesten, Jesse B. Zwart, Mark P. Stegeman, Arjan Fischer, Egil A. J. de Visser, J. Arjan G. M. Proc Biol Sci Ecology Plasmid-mediated antimicrobial resistance is a major contributor to the spread of resistance genes within bacterial communities. Successful plasmid spread depends upon a balance between plasmid fitness effects on the host and rates of horizontal transmission. While these key parameters are readily quantified in vitro, the influence of interactions with other microbiome members is largely unknown. Here, we investigated the influence of three genera of lactic acid bacteria (LAB) derived from the chicken gastrointestinal microbiome on the spread of an epidemic narrow-range ESBL resistance plasmid, IncI1 carrying bla(CTX-M-1), in mixed cultures of isogenic Escherichia coli strains. Secreted products of LAB decreased E. coli growth rates in a genus-specific manner but did not affect plasmid transfer rates. Importantly, we quantified plasmid transfer rates by controlling for density-dependent mating opportunities. Parametrization of a mathematical model with our in vitro estimates illustrated that small fitness costs of plasmid carriage may tip the balance towards plasmid loss under growth conditions in the gastrointestinal tract. This work shows that microbial interactions can influence plasmid success and provides an experimental-theoretical framework for further study of plasmid transfer in a microbiome context. The Royal Society 2021-11-10 2021-11-03 /pmc/articles/PMC8564601/ /pubmed/34727719 http://dx.doi.org/10.1098/rspb.2021.2027 Text en © 2021 The Authors. https://creativecommons.org/licenses/by/4.0/Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, provided the original author and source are credited. |
spellingShingle | Ecology Duxbury, Sarah J. N. Alderliesten, Jesse B. Zwart, Mark P. Stegeman, Arjan Fischer, Egil A. J. de Visser, J. Arjan G. M. Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title | Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title_full | Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title_fullStr | Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title_full_unstemmed | Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title_short | Chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in Escherichia coli |
title_sort | chicken gut microbiome members limit the spread of an antimicrobial resistance plasmid in escherichia coli |
topic | Ecology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8564601/ https://www.ncbi.nlm.nih.gov/pubmed/34727719 http://dx.doi.org/10.1098/rspb.2021.2027 |
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