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Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter

Evangelos Mourkas Orcid Logo, Koji Yahara Orcid Logo, Sion C Bayliss Orcid Logo, Jessica K Calland, Håkan Johansson, Leonardos Mageiros Orcid Logo, Zilia Y Muñoz-Ramirez Orcid Logo, Grant Futcher, Guillaume Méric Orcid Logo, Matthew Hitchings Orcid Logo, Santiago Sandoval-Motta, Javier Torres Orcid Logo, Keith A Jolley Orcid Logo, Martin CJ Maiden Orcid Logo, Patrik Ellström, Jonas Waldenström Orcid Logo, Ben Pascoe Orcid Logo, Samuel K Sheppard Orcid Logo

eLife, Volume: 11

Swansea University Authors: Matthew Hitchings Orcid Logo, Ben Pascoe Orcid Logo

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DOI (Published version): 10.7554/elife.73552

Abstract

Horizontal gene transfer (HGT) can allow traits that have evolved in one bacterial species to transfer to another. This has potential to rapidly promote new adaptive trajectories such as zoonotic transfer or antimicrobial resistance. However, for this to occur requires gaps to align in barriers to r...

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Published in: eLife
ISSN: 2050-084X
Published: eLife Sciences Publications, Ltd 2022
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URI: https://cronfa.swan.ac.uk/Record/cronfa59565
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spelling 2022-08-16T15:04:56.1197071 v2 59565 2022-03-09 Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter be98847c72c14a731c4a6b7bc02b3bcf 0000-0002-5527-4709 Matthew Hitchings Matthew Hitchings true false 4660c0eb7e6bfd796cd749ae713ea558 0000-0001-6376-5121 Ben Pascoe Ben Pascoe true false 2022-03-09 MEDS Horizontal gene transfer (HGT) can allow traits that have evolved in one bacterial species to transfer to another. This has potential to rapidly promote new adaptive trajectories such as zoonotic transfer or antimicrobial resistance. However, for this to occur requires gaps to align in barriers to recombination within a given time frame. Chief among these barriers is the physical separation of species with distinct ecologies in separate niches. Within the genus there are species with divergent ecologies, from rarely isolated single host specialists to multi-host generalist species that are among the most common global causes of human bacterial gastroenteritis. Here, by characterising these contrasting ecologies, we can quantify HGT among sympatric and allopatric species in natural populations. Analysing recipient and donor population ancestry among genomes from 30 species we show that cohabitation in the same host can lead to a 6-fold increase in HGT between species. This accounts for up to 30% of all SNPs within a given species and identifies highly recombinogenic genes with functions including host adaptation and antimicrobial resistance. As described in some animal and plant species, ecological factors are a major evolutionary force for speciation in bacteria and changes to the host landscape can promote partial convergence of distinct species through HGT. [Abstract copyright: © 2022, Mourkas et al.] Journal Article eLife 11 eLife Sciences Publications, Ltd 2050-084X Campylobacter, genus, species, niche, adaptation, host, evolution 22 2 2022 2022-02-22 10.7554/elife.73552 COLLEGE NANME Medical School COLLEGE CODE MEDS Swansea University This work was supported by Wellcome Trust grants 088786/C/09/Z and Medical Research Council (MRC) grants MR/M501608/1 and MR/L015080/1 awarded to SKS 2022-08-16T15:04:56.1197071 2022-03-09T14:47:27.2202886 Faculty of Medicine, Health and Life Sciences Swansea University Medical School - Medicine Evangelos Mourkas 0000-0002-7411-4743 1 Koji Yahara 0000-0003-4289-1115 2 Sion C Bayliss 0000-0002-5997-2002 3 Jessica K Calland 4 Håkan Johansson 5 Leonardos Mageiros 0000-0002-0846-522x 6 Zilia Y Muñoz-Ramirez 0000-0001-8673-0191 7 Grant Futcher 8 Guillaume Méric 0000-0001-6288-9958 9 Matthew Hitchings 0000-0002-5527-4709 10 Santiago Sandoval-Motta 11 Javier Torres 0000-0003-3945-4221 12 Keith A Jolley 0000-0002-0751-0287 13 Martin CJ Maiden 0000-0001-6321-5138 14 Patrik Ellström 15 Jonas Waldenström 0000-0002-1152-4235 16 Ben Pascoe 0000-0001-6376-5121 17 Samuel K Sheppard 0000-0001-6901-3203 18 59565__23740__0618504ea68a4a2e8d42ecf4f9a081d4.pdf 59565_VoR.pdf 2022-03-30T12:06:51.2007690 Output 1659547 application/pdf Version of Record true Copyright Mourkas et al. This article is distributed under the terms of the Creative Commons Attribution License true eng http://creativecommons.org/licenses/by/4.0/
title Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
spellingShingle Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
Matthew Hitchings
Ben Pascoe
title_short Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
title_full Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
title_fullStr Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
title_full_unstemmed Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
title_sort Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
author_id_str_mv be98847c72c14a731c4a6b7bc02b3bcf
4660c0eb7e6bfd796cd749ae713ea558
author_id_fullname_str_mv be98847c72c14a731c4a6b7bc02b3bcf_***_Matthew Hitchings
4660c0eb7e6bfd796cd749ae713ea558_***_Ben Pascoe
author Matthew Hitchings
Ben Pascoe
author2 Evangelos Mourkas
Koji Yahara
Sion C Bayliss
Jessica K Calland
Håkan Johansson
Leonardos Mageiros
Zilia Y Muñoz-Ramirez
Grant Futcher
Guillaume Méric
Matthew Hitchings
Santiago Sandoval-Motta
Javier Torres
Keith A Jolley
Martin CJ Maiden
Patrik Ellström
Jonas Waldenström
Ben Pascoe
Samuel K Sheppard
format Journal article
container_title eLife
container_volume 11
publishDate 2022
institution Swansea University
issn 2050-084X
doi_str_mv 10.7554/elife.73552
publisher eLife Sciences Publications, Ltd
college_str Faculty of Medicine, Health and Life Sciences
hierarchytype
hierarchy_top_id facultyofmedicinehealthandlifesciences
hierarchy_top_title Faculty of Medicine, Health and Life Sciences
hierarchy_parent_id facultyofmedicinehealthandlifesciences
hierarchy_parent_title Faculty of Medicine, Health and Life Sciences
department_str Swansea University Medical School - Medicine{{{_:::_}}}Faculty of Medicine, Health and Life Sciences{{{_:::_}}}Swansea University Medical School - Medicine
document_store_str 1
active_str 0
description Horizontal gene transfer (HGT) can allow traits that have evolved in one bacterial species to transfer to another. This has potential to rapidly promote new adaptive trajectories such as zoonotic transfer or antimicrobial resistance. However, for this to occur requires gaps to align in barriers to recombination within a given time frame. Chief among these barriers is the physical separation of species with distinct ecologies in separate niches. Within the genus there are species with divergent ecologies, from rarely isolated single host specialists to multi-host generalist species that are among the most common global causes of human bacterial gastroenteritis. Here, by characterising these contrasting ecologies, we can quantify HGT among sympatric and allopatric species in natural populations. Analysing recipient and donor population ancestry among genomes from 30 species we show that cohabitation in the same host can lead to a 6-fold increase in HGT between species. This accounts for up to 30% of all SNPs within a given species and identifies highly recombinogenic genes with functions including host adaptation and antimicrobial resistance. As described in some animal and plant species, ecological factors are a major evolutionary force for speciation in bacteria and changes to the host landscape can promote partial convergence of distinct species through HGT. [Abstract copyright: © 2022, Mourkas et al.]
published_date 2022-02-22T08:09:52Z
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score 11.047674

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