Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni

Evangelos Mourkas, Aidan J Taylor, Guillaume Méric, Sion C Bayliss, Ben Pascoe, Leonardos Mageiros, Jessica K Calland, Matthew D Hitchings, Anne Ridley, Ana Vidal, Ken J Forbes, Norval J C Strachan, Craig T Parker, Julian Parkhill, Keith A Jolley, Alison J Cody, Martin C J Maiden, David J Kelly* (Corresponding Author), Samuel K Sheppard* (Corresponding Author)

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

40 Citations (Scopus)
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Abstract

Modern agriculture has dramatically changed the distribution of animal species on Earth. Changes to host ecology have a major impact on the microbiota, potentially increasing the risk of zoonotic pathogens being transmitted to humans, but the impact of intensive livestock production on host-associated bacteria has rarely been studied. Here, we use large isolate collections and comparative genomics techniques, linked to phenotype studies, to understand the timescale and genomic adaptations associated with the proliferation of the most common food-born bacterial pathogen (Campylobacter jejuni) in the most prolific agricultural mammal (cattle). Our findings reveal the emergence of cattle specialist C. jejuni lineages from a background of host generalist strains that coincided with the dramatic rise in cattle numbers in the 20th century. Cattle adaptation was associated with horizontal gene transfer and significant gene gain and loss. This may be related to differences in host diet, anatomy, and physiology, leading to the proliferation of globally disseminated cattle specialists of major public health importance. This work highlights how genomic plasticity can allow important zoonotic pathogens to exploit altered niches in the face of anthropogenic change and provides information for mitigating some of the risks posed by modern agricultural systems.

Original languageEnglish
Pages (from-to)11018-11028
Number of pages11
JournalProceedings of the National Academy of Sciences of the United States of America
Volume117
Issue number20
Early online date4 May 2020
DOIs
Publication statusPublished - 19 May 2020

Bibliographical note

Acknowledgments
Research and computation were supported by Medical Research Council Grant MR/L015080/1, Wellcome Trust Grant 088786/C/09/Z), Food Standards Agency Grant FS246004, and Biotechnology and Biological Sciences Research Council (BBSRC) Grants BB/I02464X/1 and BB/R003491/1. E.M. is supported by a University of Bath Faculty of Science University Research Studentship Account (URSA) studentship. G.M. was supported by the National Institute Social Care and Health Research (NISCHR) Fellowship HF-14-13, and University of Bath core funding. J.K.C. is supported by a BBSRC Knowledge Transfer Network (KTN) PhD studentship. This work had support from the US Department of Agriculture, Agricultural Research Service Current Research Information System (CRIS) project 2030-42000-051-00D and Food Standards Scotland Grant FSS00017.

Keywords

  • Campylobacter
  • Genomics
  • Adaption
  • Evolution
  • Recombination
  • Adaptation

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