Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen

Mutation rates vary both within and between bacterial species, and understanding what drives this variation is essential for understanding the evolutionary dynamics of bacterial populations. In this study, we investigate two factors that are predicted to influence the mutation rate: ecology and geno...

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Autores principales: Gemma G. R. Murray, Andrew J. Balmer, Josephine Herbert, Nazreen F. Hadjirin, Caroline L. Kemp, Marta Matuszewska, Sebastian Bruchmann, A. S. Md. Mukarram Hossain, Marcelo Gottschalk, Alexander W. Tucker, Eric Miller, Lucy A. Weinert
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Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/c33dbcb5f57e4a9bb55867d0f062883d
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spelling oai:doaj.org-article:c33dbcb5f57e4a9bb55867d0f062883d2021-11-25T05:52:24ZMutation rate dynamics reflect ecological change in an emerging zoonotic pathogen1553-73901553-7404https://doaj.org/article/c33dbcb5f57e4a9bb55867d0f062883d2021-11-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8601623/?tool=EBIhttps://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Mutation rates vary both within and between bacterial species, and understanding what drives this variation is essential for understanding the evolutionary dynamics of bacterial populations. In this study, we investigate two factors that are predicted to influence the mutation rate: ecology and genome size. We conducted mutation accumulation experiments on eight strains of the emerging zoonotic pathogen Streptococcus suis. Natural variation within this species allows us to compare tonsil carriage and invasive disease isolates, from both more and less pathogenic populations, with a wide range of genome sizes. We find that invasive disease isolates have repeatedly evolved mutation rates that are higher than those of closely related carriage isolates, regardless of variation in genome size. Independent of this variation in overall rate, we also observe a stronger bias towards G/C to A/T mutations in isolates from more pathogenic populations, whose genomes tend to be smaller and more AT-rich. Our results suggest that ecology is a stronger correlate of mutation rate than genome size over these timescales, and that transitions to invasive disease are consistently accompanied by rapid increases in mutation rate. These results shed light on the impact that ecology can have on the adaptive potential of bacterial pathogens. Author summary Mutations are the ultimate source of all genetic variation and mutation rates vary considerably both within and between bacterial species. Understanding the drivers of this variation is important as it influences the capacity of bacteria to respond to challenges. It is particularly important for bacterial pathogens as it impacts how they respond to host immune responses and antibiotic treatments. Our study investigates how mutation rates vary within a bacterial species that has both a variable genome size and a variable ecological relationship with its host. While inter-species comparisons have found that bacterial species with smaller genomes tend to have faster mutation rates, our within-species comparisons show no evidence of a link between mutation rate and genome size. Instead, we find that strains that were involved in invasive infections have faster mutation rates than those carried asymptomatically by a host. This suggests that different factors influence mutation rate variation over different timescales, and that short-term changes are sensitive to ecological transitions. This contributes to our understanding of both the adaptive potential of pathogens, and the obstacles that bacteria have to overcome to cause disease in their host.Gemma G. R. MurrayAndrew J. BalmerJosephine HerbertNazreen F. HadjirinCaroline L. KempMarta MatuszewskaSebastian BruchmannA. S. Md. Mukarram HossainMarcelo GottschalkAlexander W. TuckerEric MillerLucy A. WeinertPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 11 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Gemma G. R. Murray
Andrew J. Balmer
Josephine Herbert
Nazreen F. Hadjirin
Caroline L. Kemp
Marta Matuszewska
Sebastian Bruchmann
A. S. Md. Mukarram Hossain
Marcelo Gottschalk
Alexander W. Tucker
Eric Miller
Lucy A. Weinert
Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
description Mutation rates vary both within and between bacterial species, and understanding what drives this variation is essential for understanding the evolutionary dynamics of bacterial populations. In this study, we investigate two factors that are predicted to influence the mutation rate: ecology and genome size. We conducted mutation accumulation experiments on eight strains of the emerging zoonotic pathogen Streptococcus suis. Natural variation within this species allows us to compare tonsil carriage and invasive disease isolates, from both more and less pathogenic populations, with a wide range of genome sizes. We find that invasive disease isolates have repeatedly evolved mutation rates that are higher than those of closely related carriage isolates, regardless of variation in genome size. Independent of this variation in overall rate, we also observe a stronger bias towards G/C to A/T mutations in isolates from more pathogenic populations, whose genomes tend to be smaller and more AT-rich. Our results suggest that ecology is a stronger correlate of mutation rate than genome size over these timescales, and that transitions to invasive disease are consistently accompanied by rapid increases in mutation rate. These results shed light on the impact that ecology can have on the adaptive potential of bacterial pathogens. Author summary Mutations are the ultimate source of all genetic variation and mutation rates vary considerably both within and between bacterial species. Understanding the drivers of this variation is important as it influences the capacity of bacteria to respond to challenges. It is particularly important for bacterial pathogens as it impacts how they respond to host immune responses and antibiotic treatments. Our study investigates how mutation rates vary within a bacterial species that has both a variable genome size and a variable ecological relationship with its host. While inter-species comparisons have found that bacterial species with smaller genomes tend to have faster mutation rates, our within-species comparisons show no evidence of a link between mutation rate and genome size. Instead, we find that strains that were involved in invasive infections have faster mutation rates than those carried asymptomatically by a host. This suggests that different factors influence mutation rate variation over different timescales, and that short-term changes are sensitive to ecological transitions. This contributes to our understanding of both the adaptive potential of pathogens, and the obstacles that bacteria have to overcome to cause disease in their host.
format article
author Gemma G. R. Murray
Andrew J. Balmer
Josephine Herbert
Nazreen F. Hadjirin
Caroline L. Kemp
Marta Matuszewska
Sebastian Bruchmann
A. S. Md. Mukarram Hossain
Marcelo Gottschalk
Alexander W. Tucker
Eric Miller
Lucy A. Weinert
author_facet Gemma G. R. Murray
Andrew J. Balmer
Josephine Herbert
Nazreen F. Hadjirin
Caroline L. Kemp
Marta Matuszewska
Sebastian Bruchmann
A. S. Md. Mukarram Hossain
Marcelo Gottschalk
Alexander W. Tucker
Eric Miller
Lucy A. Weinert
author_sort Gemma G. R. Murray
title Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
title_short Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
title_full Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
title_fullStr Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
title_full_unstemmed Mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
title_sort mutation rate dynamics reflect ecological change in an emerging zoonotic pathogen
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/c33dbcb5f57e4a9bb55867d0f062883d
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