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

Emily J. Richardson; Rodrigo Bacigalupe; Ewan M. Harrison; Lucy A. Weinert; Samantha Lycett; Manouk Vrieling; Kirsty Robb; Paul A. Hoskisson; Matthew T.G. Holden; Edward J. Feil; Gavin K. Paterson; Steven Y.C. Tong; Adebayo Shittu; Willem van Wamel; David M. Aanensen; Julian Parkhill; Sharon J. Peacock; Jukka Corander; Mark Holmes; J. Ross Fitzgerald

doi:10.1038/s41559-018-0617-0

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

Emily J. Richardson, Rodrigo Bacigalupe, Ewan M. Harrison, Lucy A. Weinert, Samantha Lycett, Manouk Vrieling, Kirsty Robb, Paul A. Hoskisson, Matthew T.G. Holden, Edward J. Feil, Gavin K. Paterson, Steven Y.C. Tong, Adebayo Shittu, Willem van Wamel, David M. Aanensen, Julian Parkhill, Sharon J. Peacock, Jukka Corander, Mark Holmes, J. Ross Fitzgerald

Research output: Contribution to journal › Article › peer-review

158 Citations (SciVal)

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-switching 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 remodelling 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.

Original language	English
Pages (from-to)	1468-1478
Number of pages	11
Journal	Nature Ecology and Evolution
Volume	2
Issue number	9
Early online date	23 Jul 2018
DOIs	https://doi.org/10.1038/s41559-018-0617-0
Publication status	Published - 1 Sept 2018

Funding

1The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK. 2Department of Medicine, University of Cambridge, Cambridge, UK. 3Department of Veterinary Medicine, University of Cambridge, Cambridge, UK. 4University of Strathclyde, Glasgow, UK. 5School of Medicine, University of St Andrews, St Andrews, UK. 6Milner Centre for Evolution, University of Bath, Bath, UK. 7Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK. 8Victorian Infectious Disease Service, The Royal Melbourne Hospital and The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Australia. 9Menzies School of Health Research, Darwin, Australia. 10Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Nigeria. 11Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands. 12Centre for Genomic Pathogen Surveillance, Hinxton, UK. 13Department of Infectious Disease Epidemiology, Imperial College London, London, UK. 14Wellcome Trust Sanger Institute, Hinxton, UK. 15London School of Hygiene and Tropical Medicine, London, UK. 16Helsinki Institute for Information Technology, Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland. 17Department of Biostatistics, University of Oslo, Oslo, Norway. 18Present address: Institute of Microbiology and Infection, University of Birmingham, Birmingham, UK. 19These authors contributed equally: Emily J. Richardson, Rodrigo Bacigalupe, Ewan M. Harrison, Lucy A. Weinert. *e-mail: [email protected]

ASJC Scopus subject areas

Ecology, Evolution, Behavior and Systematics
Ecology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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10.1038/s41559-018-0617-0

https://strathprints.strath.ac.uk/64731/

Cite this

Richardson, E. J., Bacigalupe, R., Harrison, E. M., Weinert, L. A., Lycett, S., Vrieling, M., Robb, K., Hoskisson, P. A., Holden, M. T. G., Feil, E. J., Paterson, G. K., Tong, S. Y. C., Shittu, A., van Wamel, W., Aanensen, D. M., Parkhill, J., Peacock, S. J., Corander, J., Holmes, M., & Fitzgerald, J. R. (2018). Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nature Ecology and Evolution, 2(9), 1468-1478. https://doi.org/10.1038/s41559-018-0617-0

Richardson, EJ, Bacigalupe, R, Harrison, EM, Weinert, LA, Lycett, S, Vrieling, M, Robb, K, Hoskisson, PA, Holden, MTG, Feil, EJ, Paterson, GK, Tong, SYC, Shittu, A, van Wamel, W, Aanensen, DM, Parkhill, J, Peacock, SJ, Corander, J, Holmes, M & Fitzgerald, JR 2018, 'Gene exchange drives the ecological success of a multi-host bacterial pathogen', Nature Ecology and Evolution, vol. 2, no. 9, pp. 1468-1478. https://doi.org/10.1038/s41559-018-0617-0

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

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UN SDGs

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Edward Feil

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

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UN SDGs

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Edward Feil

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