Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter

  1. Evangelos Mourkas
  2. Koji Yahara
  3. Sion C Bayliss
  4. Jessica K Calland
  5. Håkan Johansson
  6. Leonardos Mageiros
  7. Zilia Y Muñoz-Ramirez
  8. Grant Futcher
  9. Guillaume Méric
  10. Matthew D Hitchings
  11. Santiago Sandoval-Motta
  12. Javier Torres
  13. Keith A Jolley
  14. Martin CJ Maiden
  15. Patrik Ellström
  16. Jonas Waldenström
  17. Ben Pascoe
  18. Samuel K Sheppard  Is a corresponding author
  1. University of Bath, United Kingdom
  2. National Institute of Infectious Diseases, Japan
  3. Linnaeus University, Sweden
  4. Instituto Mexicano del Seguro Social, Mexico
  5. Baker Heart and Diabetes Institute, Australia
  6. Swansea University, United Kingdom
  7. University of Oxford, United Kingdom
  8. Uppsala University, Sweden

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 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 Campylobacter 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 Campylobacter 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.

Data availability

Genomes sequenced as part of other studies are archived on the Short Read Archive associated with BioProject accessions: PRJNA176480, PRJNA177352, PRJNA342755, PRJNA345429, PRJNA312235, PRJNA415188, PRJNA524300, PRJNA528879, PRJNA529798, PRJNA575343, PRJNA524315 and PRJNA689604. Additional genomes were also downloaded from NCBI [101] and pubMLST (http://pubmlst.org/campylobacter). Contiguous assemblies of all genome sequences compared are available at the public data repository Figshare (doi: 10.6084/m9.figshare.15061017) and individual project and accession numbers can be found in Supplementary Table 1.

Article and author information

Author details

  1. Evangelos Mourkas

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7411-4743
  2. Koji Yahara

    Antimicrobial Resistance Research Center, National Institute of Infectious Diseases, Tokyo, Japan
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-4289-1115
  3. Sion C Bayliss

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5997-2002
  4. Jessica K Calland

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Håkan Johansson

    Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, Kalmar, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  6. Leonardos Mageiros

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0846-522X
  7. Zilia Y Muñoz-Ramirez

    Instituto Mexicano del Seguro Social, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  8. Grant Futcher

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Guillaume Méric

    Cambridge Baker Systems Genomics Initiative, Baker Heart and Diabetes Institute, Melbourne, Australia
    Competing interests
    The authors declare that no competing interests exist.
  10. Matthew D Hitchings

    Swansea University, Swansea, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  11. Santiago Sandoval-Motta

    Instituto Mexicano del Seguro Social, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  12. Javier Torres

    Instituto Mexicano del Seguro Social, Mexico City, Mexico
    Competing interests
    The authors declare that no competing interests exist.
  13. Keith A Jolley

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  14. Martin CJ Maiden

    Department of Zoology, University of Oxford, Oxford, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6321-5138
  15. Patrik Ellström

    Department of Medical Sciences, Uppsala University, Uppsala, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  16. Jonas Waldenström

    Centre for Ecology and Evolution in Microbial Model Systems, Linnaeus University, Kalmar, Sweden
    Competing interests
    The authors declare that no competing interests exist.
  17. Ben Pascoe

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  18. Samuel K Sheppard

    Department of Biology and Biochemistry, University of Bath, Bath, United Kingdom
    For correspondence
    s.k.sheppard@bath.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6901-3203

Funding

Medical Research Council (MR/M501608/1)

  • Samuel K Sheppard

Medical Research Council (MR/L015080/1)

  • Samuel K Sheppard

Wellcome Trust (088786/C/09/Z)

  • Samuel K Sheppard

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Ben S Cooper, Mahidol University, Thailand

Version history

  1. Preprint posted: August 24, 2021 (view preprint)
  2. Received: September 2, 2021
  3. Accepted: February 20, 2022
  4. Accepted Manuscript published: February 22, 2022 (version 1)
  5. Version of Record published: March 10, 2022 (version 2)

Copyright

© 2022, Mourkas et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Evangelos Mourkas
  2. Koji Yahara
  3. Sion C Bayliss
  4. Jessica K Calland
  5. Håkan Johansson
  6. Leonardos Mageiros
  7. Zilia Y Muñoz-Ramirez
  8. Grant Futcher
  9. Guillaume Méric
  10. Matthew D Hitchings
  11. Santiago Sandoval-Motta
  12. Javier Torres
  13. Keith A Jolley
  14. Martin CJ Maiden
  15. Patrik Ellström
  16. Jonas Waldenström
  17. Ben Pascoe
  18. Samuel K Sheppard
(2022)
Host ecology regulates interspecies recombination in bacteria of the genus Campylobacter
eLife 11:e73552.
https://doi.org/10.7554/eLife.73552

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https://doi.org/10.7554/eLife.73552