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Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost

Plasmid conjugation is a major mechanism responsible for the spread of antibiotic resistance. Plasmid fitness costs are known to impact long‐term growth dynamics of microbial populations by providing plasmid‐carrying cells a relative (dis)advantage compared to plasmid‐free counterparts. Separately,...

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Autores principales: Prensky, Hannah, Gomez‐Simmonds, Angela, Uhlemann, Anne‐Catrin, Lopatkin, Allison J
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7919528/
https://www.ncbi.nlm.nih.gov/pubmed/33646643
http://dx.doi.org/10.15252/msb.20209913
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author Prensky, Hannah
Gomez‐Simmonds, Angela
Uhlemann, Anne‐Catrin
Lopatkin, Allison J
author_facet Prensky, Hannah
Gomez‐Simmonds, Angela
Uhlemann, Anne‐Catrin
Lopatkin, Allison J
author_sort Prensky, Hannah
collection PubMed
description Plasmid conjugation is a major mechanism responsible for the spread of antibiotic resistance. Plasmid fitness costs are known to impact long‐term growth dynamics of microbial populations by providing plasmid‐carrying cells a relative (dis)advantage compared to plasmid‐free counterparts. Separately, plasmid acquisition introduces an immediate, but transient, metabolic perturbation. However, the impact of these short‐term effects on subsequent growth dynamics has not previously been established. Here, we observed that de novo transconjugants grew significantly slower and/or with overall prolonged lag times, compared to lineages that had been replicating for several generations, indicating the presence of a plasmid acquisition cost. These effects were general to diverse incompatibility groups, well‐characterized and clinically captured plasmids, Gram‐negative recipient strains and species, and experimental conditions. Modeling revealed that both fitness and acquisition costs modulate overall conjugation dynamics, validated with previously published data. These results suggest that the hours immediately following conjugation may play a critical role in both short‐ and long‐term plasmid prevalence. This time frame is particularly relevant to microbiomes with high plasmid/strain diversity considered to be hot spots for conjugation.
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spelling pubmed-79195282021-03-12 Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost Prensky, Hannah Gomez‐Simmonds, Angela Uhlemann, Anne‐Catrin Lopatkin, Allison J Mol Syst Biol Articles Plasmid conjugation is a major mechanism responsible for the spread of antibiotic resistance. Plasmid fitness costs are known to impact long‐term growth dynamics of microbial populations by providing plasmid‐carrying cells a relative (dis)advantage compared to plasmid‐free counterparts. Separately, plasmid acquisition introduces an immediate, but transient, metabolic perturbation. However, the impact of these short‐term effects on subsequent growth dynamics has not previously been established. Here, we observed that de novo transconjugants grew significantly slower and/or with overall prolonged lag times, compared to lineages that had been replicating for several generations, indicating the presence of a plasmid acquisition cost. These effects were general to diverse incompatibility groups, well‐characterized and clinically captured plasmids, Gram‐negative recipient strains and species, and experimental conditions. Modeling revealed that both fitness and acquisition costs modulate overall conjugation dynamics, validated with previously published data. These results suggest that the hours immediately following conjugation may play a critical role in both short‐ and long‐term plasmid prevalence. This time frame is particularly relevant to microbiomes with high plasmid/strain diversity considered to be hot spots for conjugation. John Wiley and Sons Inc. 2021-03-01 /pmc/articles/PMC7919528/ /pubmed/33646643 http://dx.doi.org/10.15252/msb.20209913 Text en © 2021 The Authors. Published under the terms of the CC BY 4.0 license This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Prensky, Hannah
Gomez‐Simmonds, Angela
Uhlemann, Anne‐Catrin
Lopatkin, Allison J
Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title_full Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title_fullStr Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title_full_unstemmed Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title_short Conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
title_sort conjugation dynamics depend on both the plasmid acquisition cost and the fitness cost
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7919528/
https://www.ncbi.nlm.nih.gov/pubmed/33646643
http://dx.doi.org/10.15252/msb.20209913
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