Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons.


Journal

PLoS genetics
ISSN: 1553-7404
Titre abrégé: PLoS Genet
Pays: United States
ID NLM: 101239074

Informations de publication

Date de publication:
08 2023
Historique:
received: 02 02 2023
accepted: 14 06 2023
medline: 7 8 2023
pubmed: 3 8 2023
entrez: 3 8 2023
Statut: epublish

Résumé

The emergence of antibiotic resistance under treatment depends on the availability of resistance alleles and their establishment in the population. Novel resistance alleles are encoded either in chromosomal or extrachromosomal genetic elements; both types may be present in multiple copies within the cell. However, the effect of polyploidy on the emergence of antibiotic resistance remains understudied. Here we show that the establishment of resistance alleles in microbial populations depends on the ploidy level. Evolving bacterial populations under selection for antibiotic resistance, we demonstrate that resistance alleles in polyploid elements are lost frequently in comparison to alleles in monoploid elements due to segregational drift. Integrating the experiments with a mathematical model, we find a remarkable agreement between the theoretical and empirical results, confirming our understanding of the allele segregation process. Using the mathematical model, we further show that the effect of polyploidy on the establishment probability of beneficial alleles is strongest for low replicon copy numbers and plateaus for high replicon copy numbers. Our results suggest that the distribution of fitness effects for mutations that are eventually fixed in a population depends on the replicon ploidy level. Our study indicates that the emergence of antibiotic resistance in bacterial pathogens depends on the pathogen ploidy level.

Identifiants

pubmed: 37535631
doi: 10.1371/journal.pgen.1010829
pii: PGENETICS-D-23-00131
pmc: PMC10399855
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e1010829

Informations de copyright

Copyright: © 2023 Garoña et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

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Auteurs

Ana Garoña (A)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Mario Santer (M)

Institute of General Microbiology, Kiel University, Kiel, Germany.
Research group Stochastic Evolutionary Dynamics, Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Plön, Germany.

Nils F Hülter (NF)

Institute of General Microbiology, Kiel University, Kiel, Germany.

Hildegard Uecker (H)

Research group Stochastic Evolutionary Dynamics, Department of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Plön, Germany.

Tal Dagan (T)

Institute of General Microbiology, Kiel University, Kiel, Germany.

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