Emergence of methicillin resistance predates the clinical use of antibiotics

Jesper Larsen*, Claire L. Raisen, Xiaoliang Ba, Nicholas J. Sadgrove, Guillermo F. Padilla-González, Monique S. J. Simmonds, Igor Loncaric, Heidrun Kerschner, Petra Apfalter, Rainer Hartl, Ariane Deplano, Stien Vandendriessche, Barbora Černá Bolfíková, Pavel Hulva, Maiken C. Arendrup, Rasmus K. Hare, Céline Barnadas, Marc Stegger, Raphael N. Sieber, Robert L. SkovAndreas Petersen, Øystein Angen, Sophie L. Rasmussen, Carmen Espinosa-Gongora, Frank M. Aarestrup, Laura J. Lindholm, Suvi M. Nykäsenoja, Frederic Laurent, Karsten Becker, Birgit Walther, Corinna Kehrenberg, Christiane Cuny, Franziska Layer, Guido Werner, Wolfgang Witte, Ivonne Stamm, Paolo Moroni, Hannah J. Jørgensen, Hermínia de Lencastre, Emilia Cercenado, Fernando García-Garrote, Stefan Börjesson, Sara Hæggman, Vincent Perreten, Christopher J. Teale, Andrew S. Waller, Bruno Pichon, Martin D. Curran, Matthew J. Ellington, John J. Welch, Sharon J. Peacock, David J. Seilly, Fiona J. E. Morgan, Julian Parkhill, Nazreen F. Hadjirin, Jodi A. Lindsay, Matthew T. G. Holden, Giles F. Edwards, Geoffrey Foster, Gavin K. Paterson, Xavier Didelot, Mark A. Holmes, Ewan M. Harrison, Anders R. Larsen

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

32 Citations (Scopus)
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Abstract

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.
Original languageEnglish
Pages (from-to)135-141
Number of pages7
JournalNature
Volume602
Issue number7895
Early online date5 Jan 2022
DOIs
Publication statusFirst published - 5 Jan 2022

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