Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.

Measuring molecular evolution in bacteria typically requires estimation of the rate at which nucleotide changes accumulate in strains sampled at different times that share a common ancestor. This approach has been useful for dating ecological and evolutionary events that coincide with the emergence...

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Autores principales: Jessica K Calland, Ben Pascoe, Sion C Bayliss, Evangelos Mourkas, Elvire Berthenet, Harry A Thorpe, Matthew D Hitchings, Edward J Feil, Jukka Corander, Martin J Blaser, Daniel Falush, Samuel K Sheppard
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Publicado: Public Library of Science (PLoS) 2021
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Acceso en línea:https://doaj.org/article/41191db470e540458ae06371ac449ca4
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spelling oai:doaj.org-article:41191db470e540458ae06371ac449ca42021-12-02T20:03:18ZQuantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.1553-73901553-740410.1371/journal.pgen.1009829https://doaj.org/article/41191db470e540458ae06371ac449ca42021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009829https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Measuring molecular evolution in bacteria typically requires estimation of the rate at which nucleotide changes accumulate in strains sampled at different times that share a common ancestor. This approach has been useful for dating ecological and evolutionary events that coincide with the emergence of important lineages, such as outbreak strains and obligate human pathogens. However, in multi-host (niche) transmission scenarios, where the pathogen is essentially an opportunistic environmental organism, sampling is often sporadic and rarely reflects the overall population, particularly when concentrated on clinical isolates. This means that approaches that assume recent common ancestry are not applicable. Here we present a new approach to estimate the molecular clock rate in Campylobacter that draws on the popular probability conundrum known as the 'birthday problem'. Using large genomic datasets and comparative genomic approaches, we use isolate pairs that share recent common ancestry to estimate the rate of nucleotide change for the population. Identifying synonymous and non-synonymous nucleotide changes, both within and outside of recombined regions of the genome, we quantify clock-like diversification to estimate synonymous rates of nucleotide change for the common pathogenic bacteria Campylobacter coli (2.4 x 10-6 s/s/y) and Campylobacter jejuni (3.4 x 10-6 s/s/y). Finally, using estimated total rates of nucleotide change, we infer the number of effective lineages within the sample time frame-analogous to a shared birthday-and assess the rate of turnover of lineages in our sample set over short evolutionary timescales. This provides a generalizable approach to calibrating rates in populations of environmental bacteria and shows that multiple lineages are maintained, implying that large-scale clonal sweeps may take hundreds of years or more in these species.Jessica K CallandBen PascoeSion C BaylissEvangelos MourkasElvire BerthenetHarry A ThorpeMatthew D HitchingsEdward J FeilJukka CoranderMartin J BlaserDaniel FalushSamuel K SheppardPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 9, p e1009829 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Jessica K Calland
Ben Pascoe
Sion C Bayliss
Evangelos Mourkas
Elvire Berthenet
Harry A Thorpe
Matthew D Hitchings
Edward J Feil
Jukka Corander
Martin J Blaser
Daniel Falush
Samuel K Sheppard
Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
description Measuring molecular evolution in bacteria typically requires estimation of the rate at which nucleotide changes accumulate in strains sampled at different times that share a common ancestor. This approach has been useful for dating ecological and evolutionary events that coincide with the emergence of important lineages, such as outbreak strains and obligate human pathogens. However, in multi-host (niche) transmission scenarios, where the pathogen is essentially an opportunistic environmental organism, sampling is often sporadic and rarely reflects the overall population, particularly when concentrated on clinical isolates. This means that approaches that assume recent common ancestry are not applicable. Here we present a new approach to estimate the molecular clock rate in Campylobacter that draws on the popular probability conundrum known as the 'birthday problem'. Using large genomic datasets and comparative genomic approaches, we use isolate pairs that share recent common ancestry to estimate the rate of nucleotide change for the population. Identifying synonymous and non-synonymous nucleotide changes, both within and outside of recombined regions of the genome, we quantify clock-like diversification to estimate synonymous rates of nucleotide change for the common pathogenic bacteria Campylobacter coli (2.4 x 10-6 s/s/y) and Campylobacter jejuni (3.4 x 10-6 s/s/y). Finally, using estimated total rates of nucleotide change, we infer the number of effective lineages within the sample time frame-analogous to a shared birthday-and assess the rate of turnover of lineages in our sample set over short evolutionary timescales. This provides a generalizable approach to calibrating rates in populations of environmental bacteria and shows that multiple lineages are maintained, implying that large-scale clonal sweeps may take hundreds of years or more in these species.
format article
author Jessica K Calland
Ben Pascoe
Sion C Bayliss
Evangelos Mourkas
Elvire Berthenet
Harry A Thorpe
Matthew D Hitchings
Edward J Feil
Jukka Corander
Martin J Blaser
Daniel Falush
Samuel K Sheppard
author_facet Jessica K Calland
Ben Pascoe
Sion C Bayliss
Evangelos Mourkas
Elvire Berthenet
Harry A Thorpe
Matthew D Hitchings
Edward J Feil
Jukka Corander
Martin J Blaser
Daniel Falush
Samuel K Sheppard
author_sort Jessica K Calland
title Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
title_short Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
title_full Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
title_fullStr Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
title_full_unstemmed Quantifying bacterial evolution in the wild: A birthday problem for Campylobacter lineages.
title_sort quantifying bacterial evolution in the wild: a birthday problem for campylobacter lineages.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/41191db470e540458ae06371ac449ca4
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