Gene exchange drives the ecological success of a multi-host bacterial pathogen

Richardson, Emily J. and Bacigalupe, Rodrigo and Harrison, Ewan M. and Weinert, Lucy A. and Lycett, Samantha and Vrieling, Manouk and Robb, Kirsty and Hoskisson, Paul A. and Holden, Matthew TG and Feil, Edward J. and Patterson, Gavin K. and Tong, Steven YC and Shittu, Adebayo and van Wamel, Willen and Aanensen, David M. and Parkhill, Julian and Peacock, Sharon J. and Corander, Jukka and Holmes, Mark and Fitzgerald, J. Ross (2018) Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nature Ecology & Evolution, 2. 1468–1478. ISSN 2397-334X (https://doi.org/10.1038/s41559-018-0617-0)

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Abstract

The capacity for some pathogens to jump into different host-species populations is a major threat to public health and food security. Staphylococcus aureus is a multi-host bacterial pathogen responsible for important human and livestock diseases. Here, using a population genomic approach we identify humans as a major hub for ancient and recent S. aureus host-switch events linked to the emergence of endemic livestock strains, and cows as the main animal reservoir for the emergence of human epidemic clones. Such host-species transitions are associated with horizontal acquisition of genetic elements from host-specific gene pools conferring traits required for survival in the new host-niche. Importantly, genes associated with antimicrobial resistance are unevenly distributed among human and animal hosts reflecting distinct antibiotic usage practices in medicine and agriculture. In addition to gene acquisition, genetic diversification has occurred in pathways associated with nutrient acquisition, implying metabolic remodeling after a host-switch in response to distinct nutrient availability. For example, S. aureus from dairy cattle exhibit enhanced utilization of lactose, a major source of carbohydrate in bovine milk. Overall, our findings highlight the influence of human activities on the multi-host ecology of a major bacterial pathogen, underpinned by horizontal gene transfer and core genome diversification.

ORCID iDs

Richardson, Emily J., Bacigalupe, Rodrigo, Harrison, Ewan M., Weinert, Lucy A., Lycett, Samantha, Vrieling, Manouk, Robb, Kirsty ORCID logoORCID: https://orcid.org/0000-0002-7388-9782, Hoskisson, Paul A. ORCID logoORCID: https://orcid.org/0000-0003-4332-1640, Holden, Matthew TG, Feil, Edward J., Patterson, Gavin K., Tong, Steven YC, Shittu, Adebayo, van Wamel, Willen, Aanensen, David M., Parkhill, Julian, Peacock, Sharon J., Corander, Jukka, Holmes, Mark and Fitzgerald, J. Ross;
CORE (COnnecting REpositories)