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

Authors: MOURKAS, EVANGELOS - University Of Bath; TAYLOR, AIDAN - University Of Sheffield; MÉRIC, GUILLAUME - University Of Bath; BAYLISS, SION - University Of Bath; PASCOE, BEN - University Of Bath; MAGEIROS, LEONARDOS - University Of Bath; CALLAND, JESSICA - University Of Bath; RIDLEY, ANNE - Animal And Plant Health Agency; VIDAL, ANA - Animal And Plant Health Agency; FORBES, KEN - University Of Aberdeen; STRACHAN, NORVAL - University Of Aberdeen; Parker, Craig; PARKHILL, JULIAN - Cambridge University; CODY, ALISON - Oxford University; JOLLEY, KEITH - Oxford University; MAIDEN, MARTIN - Oxford University; KELLY, DAVID - University Of Sheffield; SHEPPARD, SAMUEL - University Of Bath

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/23/2020
Publication Date: 5/4/2020
Citation: Mourkas, E., Taylor, A.J., Méric, G., Bayliss, S.C., Pascoe, B., Mageiros, L., Calland, J.K., Ridley, A., Vidal, A., Forbes, K., Strachan, N.J., Parker, C., Parkhill, J., Cody, A., Jolley, K.A., Maiden, M.M., Kelly, D.J., Sheppard, S.K. 2020. Agricultural intensification and the evolution of host specialism in the enteric pathogen Campylobacter jejuni. Proceedings of the National Academy of Sciences. 117(20):11018-11028. https://doi.org/10.1073/pnas.1917168117.
DOI: https://doi.org/10.1073/pnas.1917168117

Interpretive Summary: Modern agriculture has dramatically changed the distribution of animal species on earth. Today, livestock account for 60% of all mammal biomass, with cattle being the most abundant, far surpassing the biomass of all wild mammals combined. 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 time-scale and genomic adaptations that promote proliferation of the most common food-born bacterial pathogen (C. jejuni) in the most prolific 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 facilitated by horizontal gene transfer and significant gene gain and loss, related to differences in host diet, anatomy and histology, and led to the proliferation of globally disseminated cattle specialists of major public health importance. This work highlights how the 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.

Technical 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 time-scale and genomic adaptations that promote proliferation of the most common food-born bacterial pathogen (C. jejuni) in the most prolific 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 facilitated by horizontal gene transfer and significant gene gain and loss, related to differences in host diet, anatomy and histology, and led to the proliferation of globally disseminated cattle specialists of major public health importance. This work highlights how the 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.