Emergence of methicillin resistance predates the clinical use of antibiotics
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The discovery of antibiotics more than 80 years ago has led to considerable improvements in human and animal health. Although antibiotic resistance in environmental bacteria is ancient, resistance in human pathogens is thought to be a modern phenomenon that is driven by the clinical use of antibiotics1. Here we show that particular lineages of methicillin-resistant Staphylococcus aureus—a notorious human pathogen—appeared in European hedgehogs in the pre-antibiotic era. Subsequently, these lineages spread within the local hedgehog populations and between hedgehogs and secondary hosts, including livestock and humans. We also demonstrate that the hedgehog dermatophyte Trichophyton erinacei produces two β-lactam antibiotics that provide a natural selective environment in which methicillin-resistant S. aureus isolates have an advantage over susceptible isolates. Together, these results suggest that methicillin resistance emerged in the pre-antibiotic era as a co-evolutionary adaptation of S. aureus to the colonization of dermatophyte-infected hedgehogs. The evolution of clinically relevant antibiotic-resistance genes in wild animals and the connectivity of natural, agricultural and human ecosystems demonstrate that the use of a One Health approach is critical for our understanding and management of antibiotic resistance, which is one of the biggest threats to global health, food security and development.
| Originalsprog | Engelsk |
|---|---|
| Tidsskrift | Nature |
| Vol/bind | 602 |
| Sider (fra-til) | 135–141 |
| ISSN | 0028-0836 |
| DOI | |
| Status | Udgivet - 2022 |
Bibliografisk note
Funding Information:
Acknowledgements We thank M. Ganoti, F. Attila-Zoltán, M. Dugar, Z. Pokorná, D. Madsen, S. M. Gamborg, R. Molina-López, C. Rodrigues, T. Vieira, J. Viricel, A. Fingar, K. South, G. Prince, H. Gasser, S. Sebright, N. Ennew, C. Catchpole, E. Acton, N. Acton, K. Horrey and P. Loague for providing hedgehog samples; A. Medina, L. R. H. Kildevang, P. T. Hansen, and S. M. Johansson for technical assistance during the analysis of hedgehog samples; A. E. Henius for help with Figs. 1, 4 and Extended Data Fig. 8; and V. Bortolaia for reading the manuscript. This work is dedicated to V. R. Simpson, who passed away during the study. B.Č.B. was supported by a grant from the Czech University of Life Sciences Prague (no. IGA 20213106). X.D. was funded by a grant from the National Institute for Health Research (NIHR) Health Protection Research Unit in Genomics and Enabling Data (no. NIHR200892). M.A.H. was supported by grants from the Medical Research Council (nos. G1001787/1, MR/N002660/1 and MR/P007201/1) and the Economic and Social Research Council (no. ES/S000186/1). E.M.H. was supported by a UK Research and Innovation (UKRI) Fellowship (no. MR/S00291X/1). We acknowledge Eurostat for the provision of maps, which are licensed under the Creative Commons Attribution 4.0 International (CC BY 4.0) licence, and administrative boundaries, which are copyright of EuroGeographics.
Publisher Copyright:
© 2022, The Author(s).
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