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Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics

As infectious agents of bacteria and vehicles of horizontal gene transfer, plasmids play a key role in bacterial ecology and evolution. Plasmid dynamics are shaped not only by plasmid–host interactions but also by ecological interactions between plasmid variants. These interactions are complex: plas...

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Autores principales: Igler, Claudia, Huisman, Jana S., Siedentop, Berit, Bonhoeffer, Sebastian, Lehtinen, Sonja
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628072/
https://www.ncbi.nlm.nih.gov/pubmed/34839701
http://dx.doi.org/10.1098/rstb.2020.0478
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author Igler, Claudia
Huisman, Jana S.
Siedentop, Berit
Bonhoeffer, Sebastian
Lehtinen, Sonja
author_facet Igler, Claudia
Huisman, Jana S.
Siedentop, Berit
Bonhoeffer, Sebastian
Lehtinen, Sonja
author_sort Igler, Claudia
collection PubMed
description As infectious agents of bacteria and vehicles of horizontal gene transfer, plasmids play a key role in bacterial ecology and evolution. Plasmid dynamics are shaped not only by plasmid–host interactions but also by ecological interactions between plasmid variants. These interactions are complex: plasmids can co-infect the same cell and the consequences for the co-resident plasmid can be either beneficial or detrimental. Many of the biological processes that govern plasmid co-infection—from systems that exclude infection by other plasmids to interactions in the regulation of plasmid copy number—are well characterized at a mechanistic level. Modelling plays a central role in translating such mechanistic insights into predictions about plasmid dynamics and the impact of these dynamics on bacterial evolution. Theoretical work in evolutionary epidemiology has shown that formulating models of co-infection is not trivial, as some modelling choices can introduce unintended ecological assumptions. Here, we review how the biological processes that govern co-infection can be represented in a mathematical model, discuss potential modelling pitfalls, and analyse this model to provide general insights into how co-infection impacts ecological and evolutionary outcomes. In particular, we demonstrate how beneficial and detrimental effects of co-infection give rise to frequency-dependent selection on plasmid variants. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’.
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spelling pubmed-86280722021-12-23 Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics Igler, Claudia Huisman, Jana S. Siedentop, Berit Bonhoeffer, Sebastian Lehtinen, Sonja Philos Trans R Soc Lond B Biol Sci Articles As infectious agents of bacteria and vehicles of horizontal gene transfer, plasmids play a key role in bacterial ecology and evolution. Plasmid dynamics are shaped not only by plasmid–host interactions but also by ecological interactions between plasmid variants. These interactions are complex: plasmids can co-infect the same cell and the consequences for the co-resident plasmid can be either beneficial or detrimental. Many of the biological processes that govern plasmid co-infection—from systems that exclude infection by other plasmids to interactions in the regulation of plasmid copy number—are well characterized at a mechanistic level. Modelling plays a central role in translating such mechanistic insights into predictions about plasmid dynamics and the impact of these dynamics on bacterial evolution. Theoretical work in evolutionary epidemiology has shown that formulating models of co-infection is not trivial, as some modelling choices can introduce unintended ecological assumptions. Here, we review how the biological processes that govern co-infection can be represented in a mathematical model, discuss potential modelling pitfalls, and analyse this model to provide general insights into how co-infection impacts ecological and evolutionary outcomes. In particular, we demonstrate how beneficial and detrimental effects of co-infection give rise to frequency-dependent selection on plasmid variants. This article is part of the theme issue ‘The secret lives of microbial mobile genetic elements’. The Royal Society 2022-01-17 2021-11-29 /pmc/articles/PMC8628072/ /pubmed/34839701 http://dx.doi.org/10.1098/rstb.2020.0478 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 Articles
Igler, Claudia
Huisman, Jana S.
Siedentop, Berit
Bonhoeffer, Sebastian
Lehtinen, Sonja
Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title_full Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title_fullStr Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title_full_unstemmed Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title_short Plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
title_sort plasmid co-infection: linking biological mechanisms to ecological and evolutionary dynamics
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8628072/
https://www.ncbi.nlm.nih.gov/pubmed/34839701
http://dx.doi.org/10.1098/rstb.2020.0478
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