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Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria

Parasitism creates selection for resistance mechanisms in host populations and is hypothesized to promote increased host evolvability. However, the influence of these traits on host evolution when parasites are no longer present is unclear. We used experimental evolution and whole-genome sequencing...

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Autores principales: Wielgoss, Sébastien, Bergmiller, Tobias, Bischofberger, Anna M., Hall, Alex R.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760081/
https://www.ncbi.nlm.nih.gov/pubmed/26609077
http://dx.doi.org/10.1093/molbev/msv270
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author Wielgoss, Sébastien
Bergmiller, Tobias
Bischofberger, Anna M.
Hall, Alex R.
author_facet Wielgoss, Sébastien
Bergmiller, Tobias
Bischofberger, Anna M.
Hall, Alex R.
author_sort Wielgoss, Sébastien
collection PubMed
description Parasitism creates selection for resistance mechanisms in host populations and is hypothesized to promote increased host evolvability. However, the influence of these traits on host evolution when parasites are no longer present is unclear. We used experimental evolution and whole-genome sequencing of Escherichia coli to determine the effects of past and present exposure to parasitic viruses (phages) on the spread of mutator alleles, resistance, and bacterial competitive fitness. We found that mutator alleles spread rapidly during adaptation to any of four different phage species, and this pattern was even more pronounced with multiple phages present simultaneously. However, hypermutability did not detectably accelerate adaptation in the absence of phages and recovery of fitness costs associated with resistance. Several lineages evolved phage resistance through elevated mucoidy, and during subsequent evolution in phage-free conditions they rapidly reverted to nonmucoid, phage-susceptible phenotypes. Genome sequencing revealed that this phenotypic reversion was achieved by additional genetic changes rather than by genotypic reversion of the initial resistance mutations. Insertion sequence (IS) elements played a key role in both the acquisition of resistance and adaptation in the absence of parasites; unlike single nucleotide polymorphisms, IS insertions were not more frequent in mutator lineages. Our results provide a genetic explanation for rapid reversion of mucoidy, a phenotype observed in other bacterial species including human pathogens. Moreover, this demonstrates that the types of genetic change underlying adaptation to fitness costs, and consequently the impact of evolvability mechanisms such as increased point-mutation rates, depend critically on the mechanism of resistance.
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spelling pubmed-47600812016-02-22 Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria Wielgoss, Sébastien Bergmiller, Tobias Bischofberger, Anna M. Hall, Alex R. Mol Biol Evol Discoveries Parasitism creates selection for resistance mechanisms in host populations and is hypothesized to promote increased host evolvability. However, the influence of these traits on host evolution when parasites are no longer present is unclear. We used experimental evolution and whole-genome sequencing of Escherichia coli to determine the effects of past and present exposure to parasitic viruses (phages) on the spread of mutator alleles, resistance, and bacterial competitive fitness. We found that mutator alleles spread rapidly during adaptation to any of four different phage species, and this pattern was even more pronounced with multiple phages present simultaneously. However, hypermutability did not detectably accelerate adaptation in the absence of phages and recovery of fitness costs associated with resistance. Several lineages evolved phage resistance through elevated mucoidy, and during subsequent evolution in phage-free conditions they rapidly reverted to nonmucoid, phage-susceptible phenotypes. Genome sequencing revealed that this phenotypic reversion was achieved by additional genetic changes rather than by genotypic reversion of the initial resistance mutations. Insertion sequence (IS) elements played a key role in both the acquisition of resistance and adaptation in the absence of parasites; unlike single nucleotide polymorphisms, IS insertions were not more frequent in mutator lineages. Our results provide a genetic explanation for rapid reversion of mucoidy, a phenotype observed in other bacterial species including human pathogens. Moreover, this demonstrates that the types of genetic change underlying adaptation to fitness costs, and consequently the impact of evolvability mechanisms such as increased point-mutation rates, depend critically on the mechanism of resistance. Oxford University Press 2016-03 2015-11-24 /pmc/articles/PMC4760081/ /pubmed/26609077 http://dx.doi.org/10.1093/molbev/msv270 Text en © The Author(s) 2015. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. http://creativecommons.org/licenses/by-nc/4.0/ This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact journals.permissions@oup.com
spellingShingle Discoveries
Wielgoss, Sébastien
Bergmiller, Tobias
Bischofberger, Anna M.
Hall, Alex R.
Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title_full Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title_fullStr Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title_full_unstemmed Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title_short Adaptation to Parasites and Costs of Parasite Resistance in Mutator and Nonmutator Bacteria
title_sort adaptation to parasites and costs of parasite resistance in mutator and nonmutator bacteria
topic Discoveries
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4760081/
https://www.ncbi.nlm.nih.gov/pubmed/26609077
http://dx.doi.org/10.1093/molbev/msv270
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