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Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes

Plasmids play an important role in bacterial evolution by transferring niche-adaptive functional genes between lineages, thus driving genomic diversification. Bacterial genomes commonly contain multiple, coexisting plasmid replicons, which could fuel adaptation by increasing the range of gene functi...

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Autores principales: Carrilero, Laura, Kottara, Anastasia, Guymer, David, Harrison, Ellie, Hall, James P. J., Brockhurst, Michael A.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262885/
https://www.ncbi.nlm.nih.gov/pubmed/33975933
http://dx.doi.org/10.1128/mBio.00558-21
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author Carrilero, Laura
Kottara, Anastasia
Guymer, David
Harrison, Ellie
Hall, James P. J.
Brockhurst, Michael A.
author_facet Carrilero, Laura
Kottara, Anastasia
Guymer, David
Harrison, Ellie
Hall, James P. J.
Brockhurst, Michael A.
author_sort Carrilero, Laura
collection PubMed
description Plasmids play an important role in bacterial evolution by transferring niche-adaptive functional genes between lineages, thus driving genomic diversification. Bacterial genomes commonly contain multiple, coexisting plasmid replicons, which could fuel adaptation by increasing the range of gene functions available to selection and allowing their recombination. However, plasmid coexistence is difficult to explain because the acquisition of plasmids typically incurs high fitness costs for the host cell. Here, we show that plasmid coexistence was stably maintained without positive selection for plasmid-borne gene functions and was associated with compensatory evolution to reduce fitness costs. In contrast, with positive selection, plasmid coexistence was unstable despite compensatory evolution. Positive selection discriminated between differential fitness benefits of functionally redundant plasmid replicons, retaining only the more beneficial plasmid. These data suggest that while the efficiency of negative selection against plasmid fitness costs declines over time due to compensatory evolution, positive selection to maximize plasmid-derived fitness benefits remains efficient. Our findings help to explain the forces structuring bacterial genomes: coexistence of multiple plasmids in a genome is likely to require either rare positive selection in nature or nonredundancy of accessory gene functions among the coexisting plasmids.
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spelling pubmed-82628852021-07-23 Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes Carrilero, Laura Kottara, Anastasia Guymer, David Harrison, Ellie Hall, James P. J. Brockhurst, Michael A. mBio Research Article Plasmids play an important role in bacterial evolution by transferring niche-adaptive functional genes between lineages, thus driving genomic diversification. Bacterial genomes commonly contain multiple, coexisting plasmid replicons, which could fuel adaptation by increasing the range of gene functions available to selection and allowing their recombination. However, plasmid coexistence is difficult to explain because the acquisition of plasmids typically incurs high fitness costs for the host cell. Here, we show that plasmid coexistence was stably maintained without positive selection for plasmid-borne gene functions and was associated with compensatory evolution to reduce fitness costs. In contrast, with positive selection, plasmid coexistence was unstable despite compensatory evolution. Positive selection discriminated between differential fitness benefits of functionally redundant plasmid replicons, retaining only the more beneficial plasmid. These data suggest that while the efficiency of negative selection against plasmid fitness costs declines over time due to compensatory evolution, positive selection to maximize plasmid-derived fitness benefits remains efficient. Our findings help to explain the forces structuring bacterial genomes: coexistence of multiple plasmids in a genome is likely to require either rare positive selection in nature or nonredundancy of accessory gene functions among the coexisting plasmids. American Society for Microbiology 2021-05-11 /pmc/articles/PMC8262885/ /pubmed/33975933 http://dx.doi.org/10.1128/mBio.00558-21 Text en Copyright © 2021 Carrilero et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Carrilero, Laura
Kottara, Anastasia
Guymer, David
Harrison, Ellie
Hall, James P. J.
Brockhurst, Michael A.
Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title_full Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title_fullStr Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title_full_unstemmed Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title_short Positive Selection Inhibits Plasmid Coexistence in Bacterial Genomes
title_sort positive selection inhibits plasmid coexistence in bacterial genomes
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8262885/
https://www.ncbi.nlm.nih.gov/pubmed/33975933
http://dx.doi.org/10.1128/mBio.00558-21
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