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Horizontal gene transfer and ecological interactions jointly control microbiome stability
Genes encoding resistance to stressors, such as antibiotics or environmental pollutants, are widespread across microbiomes, often encoded on mobile genetic elements. Yet, despite their prevalence, the impact of resistance genes and their mobility upon the dynamics of microbial communities remains la...
Autores principales: | , , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2022
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9678337/ https://www.ncbi.nlm.nih.gov/pubmed/36350849 http://dx.doi.org/10.1371/journal.pbio.3001847 |
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author | Coyte, Katharine Z. Stevenson, Cagla Knight, Christopher G. Harrison, Ellie Hall, James P. J. Brockhurst, Michael A. |
author_facet | Coyte, Katharine Z. Stevenson, Cagla Knight, Christopher G. Harrison, Ellie Hall, James P. J. Brockhurst, Michael A. |
author_sort | Coyte, Katharine Z. |
collection | PubMed |
description | Genes encoding resistance to stressors, such as antibiotics or environmental pollutants, are widespread across microbiomes, often encoded on mobile genetic elements. Yet, despite their prevalence, the impact of resistance genes and their mobility upon the dynamics of microbial communities remains largely unknown. Here we develop eco-evolutionary theory to explore how resistance genes alter the stability of diverse microbiomes in response to stressors. We show that adding resistance genes to a microbiome typically increases its overall stability, particularly for genes on mobile genetic elements with high transfer rates that efficiently spread resistance throughout the community. However, the impact of resistance genes upon the stability of individual taxa varies dramatically depending upon the identity of individual taxa, the mobility of the resistance gene, and the network of ecological interactions within the community. Nonmobile resistance genes can benefit susceptible taxa in cooperative communities yet damage those in competitive communities. Moreover, while the transfer of mobile resistance genes generally increases the stability of previously susceptible recipient taxa to perturbation, it can decrease the stability of the originally resistant donor taxon. We confirmed key theoretical predictions experimentally using competitive soil microcosm communities. Here the stability of a susceptible microbial community to perturbation was increased by adding mobile resistance genes encoded on conjugative plasmids but was decreased when these same genes were encoded on the chromosome. Together, these findings highlight the importance of the interplay between ecological interactions and horizontal gene transfer in driving the eco-evolutionary dynamics of diverse microbiomes. |
format | Online Article Text |
id | pubmed-9678337 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2022 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-96783372022-11-22 Horizontal gene transfer and ecological interactions jointly control microbiome stability Coyte, Katharine Z. Stevenson, Cagla Knight, Christopher G. Harrison, Ellie Hall, James P. J. Brockhurst, Michael A. PLoS Biol Research Article Genes encoding resistance to stressors, such as antibiotics or environmental pollutants, are widespread across microbiomes, often encoded on mobile genetic elements. Yet, despite their prevalence, the impact of resistance genes and their mobility upon the dynamics of microbial communities remains largely unknown. Here we develop eco-evolutionary theory to explore how resistance genes alter the stability of diverse microbiomes in response to stressors. We show that adding resistance genes to a microbiome typically increases its overall stability, particularly for genes on mobile genetic elements with high transfer rates that efficiently spread resistance throughout the community. However, the impact of resistance genes upon the stability of individual taxa varies dramatically depending upon the identity of individual taxa, the mobility of the resistance gene, and the network of ecological interactions within the community. Nonmobile resistance genes can benefit susceptible taxa in cooperative communities yet damage those in competitive communities. Moreover, while the transfer of mobile resistance genes generally increases the stability of previously susceptible recipient taxa to perturbation, it can decrease the stability of the originally resistant donor taxon. We confirmed key theoretical predictions experimentally using competitive soil microcosm communities. Here the stability of a susceptible microbial community to perturbation was increased by adding mobile resistance genes encoded on conjugative plasmids but was decreased when these same genes were encoded on the chromosome. Together, these findings highlight the importance of the interplay between ecological interactions and horizontal gene transfer in driving the eco-evolutionary dynamics of diverse microbiomes. Public Library of Science 2022-11-09 /pmc/articles/PMC9678337/ /pubmed/36350849 http://dx.doi.org/10.1371/journal.pbio.3001847 Text en © 2022 Coyte et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Coyte, Katharine Z. Stevenson, Cagla Knight, Christopher G. Harrison, Ellie Hall, James P. J. Brockhurst, Michael A. Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title | Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title_full | Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title_fullStr | Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title_full_unstemmed | Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title_short | Horizontal gene transfer and ecological interactions jointly control microbiome stability |
title_sort | horizontal gene transfer and ecological interactions jointly control microbiome stability |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9678337/ https://www.ncbi.nlm.nih.gov/pubmed/36350849 http://dx.doi.org/10.1371/journal.pbio.3001847 |
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