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Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer
The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genom...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10578598/ https://www.ncbi.nlm.nih.gov/pubmed/37792894 http://dx.doi.org/10.1371/journal.pcbi.1011532 |
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author | Pompei, Simone Bella, Edoardo Weitz, Joshua S. Grilli, Jacopo Lagomarsino, Marco Cosentino |
author_facet | Pompei, Simone Bella, Edoardo Weitz, Joshua S. Grilli, Jacopo Lagomarsino, Marco Cosentino |
author_sort | Pompei, Simone |
collection | PubMed |
description | The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genome spreads clonally within the community and together with the beneficial gene, removing genome diversity. Instead, several sources of metagenomic data show the existence of “gene-specific sweeps”, whereby a beneficial gene spreads across a bacterial community, maintaining genome diversity. Several hypotheses have been proposed to explain this process, including the decreasing gene flow between ecologically distant populations, frequency-dependent selection from linked deleterious allelles, and very high rates of horizontal gene transfer. Here, we propose an additional possible scenario grounded in eco-evolutionary principles. Specifically, we show by a mathematical model and simulations that a metacommunity where species can occupy multiple patches, acting together with a realistic (moderate) HGT rate, helps maintain genome diversity. Assuming a scenario of patches dominated by single species, our model predicts that diversity only decreases moderately upon the arrival of a new beneficial gene, and that losses in diversity can be quickly restored. We explore the generic behaviour of diversity as a function of three key parameters, frequency of insertion of new beneficial genes, migration rates and horizontal transfer rates.Our results provides a testable explanation for how diversity can be maintained by gene-specific sweeps even in the absence of high horizontal gene transfer rates. |
format | Online Article Text |
id | pubmed-10578598 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-105785982023-10-17 Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer Pompei, Simone Bella, Edoardo Weitz, Joshua S. Grilli, Jacopo Lagomarsino, Marco Cosentino PLoS Comput Biol Research Article The horizontal transfer of genes is fundamental for the eco-evolutionary dynamics of microbial communities, such as oceanic plankton, soil, and the human microbiome. In the case of an acquired beneficial gene, classic population genetics would predict a genome-wide selective sweep, whereby the genome spreads clonally within the community and together with the beneficial gene, removing genome diversity. Instead, several sources of metagenomic data show the existence of “gene-specific sweeps”, whereby a beneficial gene spreads across a bacterial community, maintaining genome diversity. Several hypotheses have been proposed to explain this process, including the decreasing gene flow between ecologically distant populations, frequency-dependent selection from linked deleterious allelles, and very high rates of horizontal gene transfer. Here, we propose an additional possible scenario grounded in eco-evolutionary principles. Specifically, we show by a mathematical model and simulations that a metacommunity where species can occupy multiple patches, acting together with a realistic (moderate) HGT rate, helps maintain genome diversity. Assuming a scenario of patches dominated by single species, our model predicts that diversity only decreases moderately upon the arrival of a new beneficial gene, and that losses in diversity can be quickly restored. We explore the generic behaviour of diversity as a function of three key parameters, frequency of insertion of new beneficial genes, migration rates and horizontal transfer rates.Our results provides a testable explanation for how diversity can be maintained by gene-specific sweeps even in the absence of high horizontal gene transfer rates. Public Library of Science 2023-10-04 /pmc/articles/PMC10578598/ /pubmed/37792894 http://dx.doi.org/10.1371/journal.pcbi.1011532 Text en © 2023 Pompei 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 Pompei, Simone Bella, Edoardo Weitz, Joshua S. Grilli, Jacopo Lagomarsino, Marco Cosentino Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title | Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title_full | Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title_fullStr | Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title_full_unstemmed | Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title_short | Metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
title_sort | metacommunity structure preserves genome diversity in the presence of gene-specific selective sweeps under moderate rates of horizontal gene transfer |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10578598/ https://www.ncbi.nlm.nih.gov/pubmed/37792894 http://dx.doi.org/10.1371/journal.pcbi.1011532 |
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