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

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-associat...

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Autores principales: Mourkas, Evangelos, Taylor, Aidan J., Méric, Guillaume, Bayliss, Sion C., Pascoe, Ben, Mageiros, Leonardos, Calland, Jessica K., Hitchings, Matthew D., Ridley, Anne, Vidal, Ana, Forbes, Ken J., Strachan, Norval J. C., Parker, Craig T., Parkhill, Julian, Jolley, Keith A., Cody, Alison J., Maiden, Martin C. J., Kelly, David J., Sheppard, Samuel K.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: National Academy of Sciences 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7245135/
https://www.ncbi.nlm.nih.gov/pubmed/32366649
http://dx.doi.org/10.1073/pnas.1917168117
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author Mourkas, Evangelos
Taylor, Aidan J.
Méric, Guillaume
Bayliss, Sion C.
Pascoe, Ben
Mageiros, Leonardos
Calland, Jessica K.
Hitchings, Matthew D.
Ridley, Anne
Vidal, Ana
Forbes, Ken J.
Strachan, Norval J. C.
Parker, Craig T.
Parkhill, Julian
Jolley, Keith A.
Cody, Alison J.
Maiden, Martin C. J.
Kelly, David J.
Sheppard, Samuel K.
author_facet Mourkas, Evangelos
Taylor, Aidan J.
Méric, Guillaume
Bayliss, Sion C.
Pascoe, Ben
Mageiros, Leonardos
Calland, Jessica K.
Hitchings, Matthew D.
Ridley, Anne
Vidal, Ana
Forbes, Ken J.
Strachan, Norval J. C.
Parker, Craig T.
Parkhill, Julian
Jolley, Keith A.
Cody, Alison J.
Maiden, Martin C. J.
Kelly, David J.
Sheppard, Samuel K.
author_sort Mourkas, Evangelos
collection PubMed
description 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.
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spelling pubmed-72451352020-06-04 Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni Mourkas, Evangelos Taylor, Aidan J. Méric, Guillaume Bayliss, Sion C. Pascoe, Ben Mageiros, Leonardos Calland, Jessica K. Hitchings, Matthew D. Ridley, Anne Vidal, Ana Forbes, Ken J. Strachan, Norval J. C. Parker, Craig T. Parkhill, Julian Jolley, Keith A. Cody, Alison J. Maiden, Martin C. J. Kelly, David J. Sheppard, Samuel K. Proc Natl Acad Sci U S A Biological Sciences 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. National Academy of Sciences 2020-05-19 2020-05-04 /pmc/articles/PMC7245135/ /pubmed/32366649 http://dx.doi.org/10.1073/pnas.1917168117 Text en Copyright © 2020 the Author(s). Published by PNAS. http://creativecommons.org/licenses/by/4.0/ https://creativecommons.org/licenses/by/4.0/This open access article is distributed under Creative Commons Attribution License 4.0 (CC BY) (http://creativecommons.org/licenses/by/4.0/) .
spellingShingle Biological Sciences
Mourkas, Evangelos
Taylor, Aidan J.
Méric, Guillaume
Bayliss, Sion C.
Pascoe, Ben
Mageiros, Leonardos
Calland, Jessica K.
Hitchings, Matthew D.
Ridley, Anne
Vidal, Ana
Forbes, Ken J.
Strachan, Norval J. C.
Parker, Craig T.
Parkhill, Julian
Jolley, Keith A.
Cody, Alison J.
Maiden, Martin C. J.
Kelly, David J.
Sheppard, Samuel K.
Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title_full Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title_fullStr Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title_full_unstemmed Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title_short Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni
title_sort agricultural intensification and the evolution of host specialism in the enteric pathogen campylobacter jejuni
topic Biological Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7245135/
https://www.ncbi.nlm.nih.gov/pubmed/32366649
http://dx.doi.org/10.1073/pnas.1917168117
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