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

Nature Ecology & Evolution volume 2, pages 1468–1478 (2018)Cite this article

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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-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.

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Fig. 1: S. aureus phylogeny according to host-species origin.
Fig. 2: S. aureus has undergone extensive ancient and recent host-switching events, with humans acting as a major hub.
Fig. 3: Network analysis of the S. aureus accessory genome indicates clustering according to host-species group.
Fig. 4: Identification of horizontally acquired genetic elements correlated with host adaptation.
Fig. 5: Summary of biological pathways under positive selection in different host species, and evidence for phenotypic adaptation.
Fig. 6: Resistance to antimicrobials is non-randomly associated with host species.

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Acknowledgements

This study was supported by a project grant (BB/I013873/1) and institute strategic grant funding ISP2: BBS/E/D/20002173 from the Biotechnology and Biological Sciences Research Council (UK) to J.R.F., Medical Research Council (UK) grant MRNO2995X/1 to J.R.F. and Wellcome Trust collaborative award 201531/Z/16/Z to J.R.F. S.Y.C.T. is an Australian National Health and Medical Research Council Career Development Fellow (number 1065736). L.A.W. is supported by a Dorothy Hodgkin Fellowship funded by the Royal Society (grant number DH140195) and a Sir Henry Dale Fellowship jointly funded by the Wellcome Trust and Royal Society (grant number 109385/Z/15/Z). S.L. is supported by a Chancellor’s Fellowship from the University of Edinburgh. M.T.G.H. was supported by the Scottish Infection Research Network and Chief Scientist Office through Scottish Healthcare Associated Infection Prevention Institute consortium funding (CSO reference: SIRN10). E.M.H. and S.J.P. were funded by The Health Innovation Challenge Fund (WT098600, HICF-T5-342), a parallel funding partnership between the Department of Health and Wellcome Trust, the UKCRC Translational Infection Research Initiative, and the Medical Research Council (grant number G1000803). S.J.P. is a National Institute for Health Research senior investigator. P.A.H. is supported by Natural Environment Research Council grant NE/M001415/1. We thank B. Blane, N. Brown and E. Torok for their role in the original study isolating and sequencing S. aureus from patients at the Cambridge University Hospitals NHS Foundation Trust, from which 76 genomes were downloaded from the ENA and used in this study. We also thank Edinburgh Genomics for sequencing, and all those who made isolates available for the study, including the Zoological Society London, G. Foster, H. Hasman, S. Monecke, E. Smith, D. Smyth and H. Jorgensen.

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Author notes

  1. Emily J. Richardson

    Present address: Institute of Microbiology and Infection, University of Birmingham, Birmingham, UK

  2. These authors contributed equally: Emily J. Richardson, Rodrigo Bacigalupe, Ewan M. Harrison, Lucy A. Weinert.

Authors and Affiliations

  1. The Roslin Institute, Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK

    Emily J. Richardson, Rodrigo Bacigalupe, Samantha Lycett, Manouk Vrieling & J. Ross Fitzgerald

  2. Department of Medicine, University of Cambridge, Cambridge, UK

    Ewan M. Harrison

  3. Department of Veterinary Medicine, University of Cambridge, Cambridge, UK

    Lucy A. Weinert & Mark Holmes

  4. University of Strathclyde, Glasgow, UK

    Kirsty Robb & Paul A. Hoskisson

  5. School of Medicine, University of St Andrews, St Andrews, UK

    Matthew T. G. Holden

  6. Milner Centre for Evolution, University of Bath, Bath, UK

    Edward J. Feil

  7. Royal (Dick) School of Veterinary Studies, University of Edinburgh, Edinburgh, UK

    Gavin K. Paterson

  8. Victorian Infectious Disease Service, The Royal Melbourne Hospital and The University of Melbourne at the Peter Doherty Institute for Infection and Immunity, Melbourne, Australia

    Steven Y. C. Tong

  9. Menzies School of Health Research, Darwin, Australia

    Steven Y. C. Tong

  10. Department of Microbiology, Obafemi Awolowo University, Ile-Ife, Nigeria

    Adebayo Shittu

  11. Department of Medical Microbiology and Infectious Diseases, Erasmus MC, Rotterdam, The Netherlands

    Willem van Wamel

  12. Centre for Genomic Pathogen Surveillance, Hinxton, UK

    David M. Aanensen

  13. Department of Infectious Disease Epidemiology, Imperial College London, London, UK

    David M. Aanensen

  14. Wellcome Trust Sanger Institute, Hinxton, UK

    Julian Parkhill & Jukka Corander

  15. London School of Hygiene and Tropical Medicine, London, UK

    Sharon J. Peacock

  16. Helsinki Institute for Information Technology, Department of Mathematics and Statistics, University of Helsinki, Helsinki, Finland

    Jukka Corander

  17. Department of Biostatistics, University of Oslo, Oslo, Norway

    Jukka Corander

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  1. Emily J. Richardson
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Contributions

J.R.F., S.J.P., J.P., M.H., E.M.H., L.A.W. and M.T.G.H. conceived and designed the study. E.J.R., R.B., E.M.H., L.A.W., S.L., M.V. and K.R. carried out the experiments. E.J.R., R.B., E.M.H., L.A.W., S.L., G.K.P., D.M.A., M.T.G.H., E.J.F., J.C., M.V., P.A.H., K.R. and J.R.F. analysed the data. S.Y.C.T., A.S. and W.v.W. provided isolates. E.J.R., R.B., E.M.H., S.L. and J.R.F. wrote the manuscript. All authors contributed to editing the manuscript.

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Correspondence to J. Ross Fitzgerald.

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Supplementary Information

Supplementary Information

Supplementary Figures 1–19; Supplementary Tables 1–12; Supplementary Notes

Reporting Summary

Supplementary Table 1

Metadata for all S. aureus isolates examined in the current study

Supplementary Table 5

Number of host jumps and transition rates between host-species groups and confidence intervals for all approaches used

Supplementary Table 6

Accessory genes enriched in isolates according to host-species or gain/loss of genes correlated with host-switching events

Supplementary Table 8

Functional groups of pseudogenes enriched in S. aureus by host-species

Supplementary Table 11

Functional categories (GO terms) of genes under positive selection in different host species

Supplementary Table 12

Distribution of antimicrobial resistance determinants according to host-species group

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Richardson, E.J., Bacigalupe, R., Harrison, E.M. et al. Gene exchange drives the ecological success of a multi-host bacterial pathogen. Nat Ecol Evol 2, 1468–1478 (2018). https://doi.org/10.1038/s41559-018-0617-0

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