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Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition

Bacteriophages (“phages”) are hypothesized to be key drivers of bacterial population dynamics, driving microbial community composition, but empirical support for this is mixed. One reason why phages may have a less-than-expected impact on community composition is that many different phages and other...

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Autores principales: Castledine, Meaghan, Newbury, Arthur, Lewis, Rai, Hacker, Christian, Meaden, Sean, Buckling, Angus
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127636/
https://www.ncbi.nlm.nih.gov/pubmed/37022158
http://dx.doi.org/10.1128/mbio.00460-23
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author Castledine, Meaghan
Newbury, Arthur
Lewis, Rai
Hacker, Christian
Meaden, Sean
Buckling, Angus
author_facet Castledine, Meaghan
Newbury, Arthur
Lewis, Rai
Hacker, Christian
Meaden, Sean
Buckling, Angus
author_sort Castledine, Meaghan
collection PubMed
description Bacteriophages (“phages”) are hypothesized to be key drivers of bacterial population dynamics, driving microbial community composition, but empirical support for this is mixed. One reason why phages may have a less-than-expected impact on community composition is that many different phages and other mobile genetic elements (MGEs) interact with each bacterium. For instance, the same phage may have higher or lower costs to different bacterial strains or species. Assuming that resistance or susceptibility to MGE infection is not consistent across all MGEs, a simple prediction is that the net effect of MGEs on each bacterial taxon may converge with an increasing number of interactions with different MGEs. We formalized this prediction using in silico population dynamics simulations and then carried out experiments using three bacterial species, one generalist conjugative plasmid, and three species-specific phages. While the presence of only phages or only the plasmid altered community structure, these differential effects on community structure canceled out when both were together. The effects of MGEs were largely indirect and could not be explained by simple pairwise bipartite interactions (i.e., between each MGE and each bacterial species). Our results suggest that the effects of MGEs may be overestimated by studies that focus on a single MGE and not on interactions among multiple MGEs.
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spelling pubmed-101276362023-04-26 Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition Castledine, Meaghan Newbury, Arthur Lewis, Rai Hacker, Christian Meaden, Sean Buckling, Angus mBio Research Article Bacteriophages (“phages”) are hypothesized to be key drivers of bacterial population dynamics, driving microbial community composition, but empirical support for this is mixed. One reason why phages may have a less-than-expected impact on community composition is that many different phages and other mobile genetic elements (MGEs) interact with each bacterium. For instance, the same phage may have higher or lower costs to different bacterial strains or species. Assuming that resistance or susceptibility to MGE infection is not consistent across all MGEs, a simple prediction is that the net effect of MGEs on each bacterial taxon may converge with an increasing number of interactions with different MGEs. We formalized this prediction using in silico population dynamics simulations and then carried out experiments using three bacterial species, one generalist conjugative plasmid, and three species-specific phages. While the presence of only phages or only the plasmid altered community structure, these differential effects on community structure canceled out when both were together. The effects of MGEs were largely indirect and could not be explained by simple pairwise bipartite interactions (i.e., between each MGE and each bacterial species). Our results suggest that the effects of MGEs may be overestimated by studies that focus on a single MGE and not on interactions among multiple MGEs. American Society for Microbiology 2023-04-06 /pmc/articles/PMC10127636/ /pubmed/37022158 http://dx.doi.org/10.1128/mbio.00460-23 Text en Copyright © 2023 Castledine 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
Castledine, Meaghan
Newbury, Arthur
Lewis, Rai
Hacker, Christian
Meaden, Sean
Buckling, Angus
Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title_full Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title_fullStr Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title_full_unstemmed Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title_short Antagonistic Mobile Genetic Elements Can Counteract Each Other’s Effects on Microbial Community Composition
title_sort antagonistic mobile genetic elements can counteract each other’s effects on microbial community composition
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10127636/
https://www.ncbi.nlm.nih.gov/pubmed/37022158
http://dx.doi.org/10.1128/mbio.00460-23
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