Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock

Gonzalo Yebra; Joshua D Harling-Lee; Samantha Lycett; Frank M Aarestrup; Gunhild Larsen; Lina M Cavaco; Keun Seok Seo; Sam Abraham; Jacqueline M Norris; Tracy Schmidt; Marthie M Ehlers; Daniel O Sordelli; Fernanda R Buzzola; Wondwossen A Gebreyes; Juliano L Gonçalves; Marcos V Dos Santos; Zunita Zakaria; Vera L M Rall; Orla M Keane; Dagmara A Niedziela; Gavin K Paterson; Mark A Holmes; Tom C Freeman; J Ross Fitzgerald

doi:10.1073/pnas.2211217119

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Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock

Journal article

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Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock

Gonzalo Yebra, Joshua D Harling-Lee, Samantha Lycett, Frank M Aarestrup, Gunhild Larsen, Lina M Cavaco, Keun Seok Seo, Sam Abraham, Jacqueline M Norris, Tracy Schmidt, …

Proceedings of the National Academy of Sciences - PNAS, Vol.119(50), e2211217119

2022

DOI: https://doi.org/10.1073/pnas.2211217119

PMID: 36469788

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Abstract

Staphylococcus aureus

agriculture

host adaptation

phylodynamics

population genomics

Most new pathogens of humans and animals arise via switching events from distinct host species. However, our understanding of the evolutionary and ecological drivers of successful host adaptation, expansion, and dissemination are limited. Staphylococcus aureus is a major bacterial pathogen of humans and a leading cause of mastitis in dairy cows worldwide. Here we trace the evolutionary history of bovine S. aureus using a global dataset of 10,254 S. aureus genomes including 1,896 bovine isolates from 32 countries in 6 continents. We identified 7 major contemporary endemic clones of S. aureus causing bovine mastitis around the world and traced them back to 4 independent host-jump events from humans that occurred up to 2,500 y ago. Individual clones emerged and underwent clonal expansion from the mid-19th to late 20th century coinciding with the commercialization and industrialization of dairy farming, and older lineages have become globally distributed via established cattle trade links. Importantly, we identified lineage-dependent differences in the frequency of host transmission events between humans and cows in both directions revealing high risk clones threatening veterinary and human health. Finally, pangenome network analysis revealed that some bovine S. aureus lineages contained distinct sets of bovine-associated genes, consistent with multiple trajectories to host adaptation via gene acquisition. Taken together, we have dissected the evolutionary history of a major endemic pathogen of livestock providing a comprehensive temporal, geographic, and gene-level perspective of its remarkable success.

Details

Title: Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock
Authors/Creators: Gonzalo Yebra (Author) - University of Edinburgh
Joshua D Harling-Lee (Author) - University of Edinburgh
Samantha Lycett (Contributor) - University of Edinburgh
Frank M Aarestrup (Contributor) - Technical University of Denmark
Gunhild Larsen (Contributor) - Technical University of Denmark
Lina M Cavaco (Contributor) - Statens Serum Institut
Keun Seok Seo (Contributor) - Mississippi State University
Sam Abraham (Contributor) - Murdoch University
Jacqueline M Norris (Contributor) - The University of Sydney
Tracy Schmidt (Contributor) - University of Pretoria
Marthie M Ehlers (Contributor) - University of Pretoria
Daniel O Sordelli (Contributor) - Consejo Nacional de Investigaciones Científicas y Técnicas
Fernanda R Buzzola (Contributor) - Consejo Nacional de Investigaciones Científicas y Técnicas
Wondwossen A Gebreyes (Contributor) - The Ohio State University
Juliano L Gonçalves (Contributor) - Universidade de São Paulo
Marcos V Dos Santos (Contributor) - Universidade de São Paulo
Zunita Zakaria (Contributor) - Universiti Putra Malaysia
Vera L M Rall (Contributor) - Universidade Estadual Paulista (Unesp)
Orla M Keane (Contributor) - Teagasc - The Irish Agriculture and Food Development Authority
Dagmara A Niedziela (Contributor) - Teagasc - The Irish Agriculture and Food Development Authority
Gavin K Paterson (Contributor) - Roslin Institute
Mark A Holmes (Contributor) - University of Cambridge
Tom C Freeman (Contributor) - Roslin Institute
J Ross Fitzgerald (Author) - Roslin Institute
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.119(50), e2211217119
Publisher: PNAS
Grant note: Wellcome Trust (201531/Z/16/Z) UKRI | Biotechnology and Biological Sciences Research Council (BB/P013740/1)
Identifiers: 991005579428607891
Murdoch Affiliation: Centre for Biosecurity and One Health; Antimicrobial Resistance and Infectious Disease Laboratory; School of Medical, Molecular and Forensic Sciences
Language: English
Resource Type: Journal article

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Collaboration types: Domestic collaboration; International collaboration
Citation topics: 1 Clinical & Life Sciences; 1.23 Antibiotics & Antimicrobials; 1.23.173 MRSA and VRE
Web Of Science research areas: Microbiology
ESI research areas: Microbiology