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Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons
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...
Autores principales: | , , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
Public Library of Science
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399855/ https://www.ncbi.nlm.nih.gov/pubmed/37535631 http://dx.doi.org/10.1371/journal.pgen.1010829 |
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author | Garoña, Ana Santer, Mario Hülter, Nils F. Uecker, Hildegard Dagan, Tal |
author_facet | Garoña, Ana Santer, Mario Hülter, Nils F. Uecker, Hildegard Dagan, Tal |
author_sort | Garoña, Ana |
collection | PubMed |
description | 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. |
format | Online Article Text |
id | pubmed-10399855 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | Public Library of Science |
record_format | MEDLINE/PubMed |
spelling | pubmed-103998552023-08-04 Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons Garoña, Ana Santer, Mario Hülter, Nils F. Uecker, Hildegard Dagan, Tal PLoS Genet Research Article 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. Public Library of Science 2023-08-03 /pmc/articles/PMC10399855/ /pubmed/37535631 http://dx.doi.org/10.1371/journal.pgen.1010829 Text en © 2023 Garoña et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. |
spellingShingle | Research Article Garoña, Ana Santer, Mario Hülter, Nils F. Uecker, Hildegard Dagan, Tal Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title | Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title_full | Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title_fullStr | Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title_full_unstemmed | Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title_short | Segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
title_sort | segregational drift hinders the evolution of antibiotic resistance on polyploid replicons |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10399855/ https://www.ncbi.nlm.nih.gov/pubmed/37535631 http://dx.doi.org/10.1371/journal.pgen.1010829 |
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