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Rapid host switching in generalist Campylobacter strains erodes the signal for tracing human infections.

Published version
Peer-reviewed

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Article

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Authors

Dearlove, Bethany L  ORCID logo  https://orcid.org/0000-0003-3653-4592
Cody, Alison J 
Méric, Guillaume 
Wilson, Daniel J 

Abstract

Campylobacter jejuni and Campylobacter coli are the biggest causes of bacterial gastroenteritis in the developed world, with human infections typically arising from zoonotic transmission associated with infected meat. Because Campylobacter is not thought to survive well outside the gut, host-associated populations are genetically isolated to varying degrees. Therefore, the likely origin of most strains can be determined by host-associated variation in the genome. This is instructive for characterizing the source of human infection. However, some common strains, notably isolates belonging to the ST-21, ST-45 and ST-828 clonal complexes, appear to have broad host ranges, hindering source attribution. Here whole-genome sequencing has the potential to reveal fine-scale genetic structure associated with host specificity. We found that rates of zoonotic transmission among animal host species in these clonal complexes were so high that the signal of host association is all but obliterated, estimating one zoonotic transmission event every 1.6, 1.8 and 12 years in the ST-21, ST-45 and ST828 complexes, respectively. We attributed 89% of clinical cases to a chicken source, 10% to cattle and 1% to pig. Our results reveal that common strains of C. jejuni and C. coli infectious to humans are adapted to a generalist lifestyle, permitting rapid transmission between different hosts. Furthermore, they show that the weak signal of host association within these complexes presents a challenge for pinpointing the source of clinical infections, underlining the view that whole-genome sequencing, powerful though it is, cannot substitute for intensive sampling of suspected transmission reservoirs.

Description

Keywords

Animals, Campylobacter, Campylobacter Infections, Cattle, Cattle Diseases, Chickens, Host Specificity, Humans, Poultry Diseases, Swine, Swine Diseases

Journal Title

ISME J

Conference Name

Journal ISSN

1751-7362
1751-7370

Volume Title

10

Publisher

Oxford University Press (OUP)
Sponsorship
Medical Research Council (MR/J013862/1)
Medical Research Council (G0800778)
This study was supported by the Oxford NIHR Biomedical Research Centre and the UKCRC Modernising Medical Microbiology Consortium, the latter funded under the UKCRC Translational Infection Research Initiative supported by the Medical Research Council, the Biotechnology and Biological Sciences Research Council and the National Institute for Health Research on behalf of the UK Department of Health (Grant G0800778) and the Wellcome Trust (Grant 087646/Z/08/Z). BLD is supported by a Medical Research Council Methodology Research Programme grant (grant number MR/J013862/1). AJC was supported by the United Kingdom Department for Environment, Food, and Rural Affairs and Food Standards Agency (grant number OZ0624). DJW is a Sir Henry Dale Fellow, jointly funded by the Wellcome Trust and the Royal Society (Grant 101237/Z/13/Z). SKS is funded by the Biotechnology and Biological Sciences Research Council (BBSRC), the Medical Research Council (MR/L015080/1) and the Wellcome Trust. This publication made use of the Campylobacter Multi Locus Sequence Typing website (http://pubmlst.org/ campylobacter/) developed by Keith Jolley and sited at the University of Oxford (24). The development of this site has been funded by the Wellcome Trust.