Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock
Autor(a) principal: | |
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Data de Publicação: | 2022 |
Outros Autores: | , , , , , , , , , , , , , , , , , , , , , , |
Tipo de documento: | Artigo |
Idioma: | eng |
Título da fonte: | Repositório Institucional da UNESP |
Texto Completo: | http://dx.doi.org/10.1073/pnas.2211217119 http://hdl.handle.net/11449/247996 |
Resumo: | 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. |
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Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestockagriculturehost adaptationphylodynamicspopulation genomicsStaphylococcus aureusMost 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.The Roslin Institute University of EdinburghThe National Food Institute Technical University of DenmarkDepartment for Bacteria Parasites and Fungi Reference Laboratory for Antimicrobial Resistance Statens Serum InstitutDepartment of Basic Sciences College of Veterinary Medicine Mississippi State UniversityCollege of Science Health Engineering and Education Antimicrobial Resistance and Infectious Diseases Laboratory Murdoch UniversitySydney School of Veterinary Science University of SydneyDepartment of Medical Microbiology University of PretoriaDepartment of Medical Microbiology Tshwane Academic Division National Health Laboratory ServiceInstituto de Investigaciones en Microbiología y Parasitología Médica University of Buenos Aires-CONICETMolecular Epidemiology College of Veterinary Medicine Ohio State UniversityDepartment of Large Animal Clinical Sciences College of Veterinary Medicine Michigan State UniversityDepartment of Nutrition and Animal Production School of Veterinary Medicine and Animal Sciences University of São Paulo, SPInstitute of Bioscience Universiti Putra Malaysia, SelangorDepartment of Microbiology and Immunology Institute of Biosciences São Paulo State University, SPAnimal & Bioscience Department, Teagasc, Grange, DunsanyThe Royal (Dick) School of Veterinary Studies University of EdinburghDepartment of Veterinary Medicine University of CambridgeJanssen ImmunologyDepartment of Microbiology and Immunology Institute of Biosciences São Paulo State University, SPUniversity of EdinburghTechnical University of DenmarkStatens Serum InstitutMississippi State UniversityMurdoch UniversityUniversity of SydneyUniversity of PretoriaNational Health Laboratory ServiceUniversity of Buenos Aires-CONICETOhio State UniversityMichigan State UniversityUniversidade de São Paulo (USP)Universiti Putra MalaysiaUniversidade Estadual Paulista (UNESP)Animal & Bioscience DepartmentUniversity of CambridgeJanssen ImmunologyYebra, GonzaloHarling-Lee, Joshua D.Lycett, SamanthaAarestrup, Frank M.Larsen, GunhildCavaco, Lina M.Seo, Keun SeokAbraham, SamNorris, Jacqueline M.Schmidt, TracyEhlers, Marthie M.Sordelli, Daniel O.Buzzola, Fernanda R.Gebreyes, Wondwossen A.Gonçalves, Juliano L.dos Santos, Marcos V.Zakaria, ZunitaRall, Vera L.M. [UNESP]Keane, Orla M.Niedziela, Dagmara A.Paterson, Gavin K.Holmes, Mark A.Freeman, Tom C.Fitzgerald, J. Ross2023-07-29T13:31:36Z2023-07-29T13:31:36Z2022-12-13info:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articlehttp://dx.doi.org/10.1073/pnas.2211217119Proceedings of the National Academy of Sciences of the United States of America, v. 119, n. 50, 2022.1091-64900027-8424http://hdl.handle.net/11449/24799610.1073/pnas.22112171192-s2.0-85143447921Scopusreponame:Repositório Institucional da UNESPinstname:Universidade Estadual Paulista (UNESP)instacron:UNESPengProceedings of the National Academy of Sciences of the United States of Americainfo:eu-repo/semantics/openAccess2023-07-29T13:31:36Zoai:repositorio.unesp.br:11449/247996Repositório InstitucionalPUBhttp://repositorio.unesp.br/oai/requestopendoar:29462024-08-05T20:56:53.623860Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP)false |
dc.title.none.fl_str_mv |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
title |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
spellingShingle |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock Yebra, Gonzalo agriculture host adaptation phylodynamics population genomics Staphylococcus aureus |
title_short |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
title_full |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
title_fullStr |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
title_full_unstemmed |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
title_sort |
Multiclonal human origin and global expansion of an endemic bacterial pathogen of livestock |
author |
Yebra, Gonzalo |
author_facet |
Yebra, Gonzalo Harling-Lee, Joshua D. Lycett, Samantha Aarestrup, Frank M. Larsen, Gunhild Cavaco, Lina M. Seo, Keun Seok Abraham, Sam Norris, Jacqueline M. Schmidt, Tracy Ehlers, Marthie M. Sordelli, Daniel O. Buzzola, Fernanda R. Gebreyes, Wondwossen A. Gonçalves, Juliano L. dos Santos, Marcos V. Zakaria, Zunita Rall, Vera L.M. [UNESP] Keane, Orla M. Niedziela, Dagmara A. Paterson, Gavin K. Holmes, Mark A. Freeman, Tom C. Fitzgerald, J. Ross |
author_role |
author |
author2 |
Harling-Lee, Joshua D. Lycett, Samantha Aarestrup, Frank M. Larsen, Gunhild Cavaco, Lina M. Seo, Keun Seok Abraham, Sam Norris, Jacqueline M. Schmidt, Tracy Ehlers, Marthie M. Sordelli, Daniel O. Buzzola, Fernanda R. Gebreyes, Wondwossen A. Gonçalves, Juliano L. dos Santos, Marcos V. Zakaria, Zunita Rall, Vera L.M. [UNESP] Keane, Orla M. Niedziela, Dagmara A. Paterson, Gavin K. Holmes, Mark A. Freeman, Tom C. Fitzgerald, J. Ross |
author2_role |
author author author author author author author author author author author author author author author author author author author author author author author |
dc.contributor.none.fl_str_mv |
University of Edinburgh Technical University of Denmark Statens Serum Institut Mississippi State University Murdoch University University of Sydney University of Pretoria National Health Laboratory Service University of Buenos Aires-CONICET Ohio State University Michigan State University Universidade de São Paulo (USP) Universiti Putra Malaysia Universidade Estadual Paulista (UNESP) Animal & Bioscience Department University of Cambridge Janssen Immunology |
dc.contributor.author.fl_str_mv |
Yebra, Gonzalo Harling-Lee, Joshua D. Lycett, Samantha Aarestrup, Frank M. Larsen, Gunhild Cavaco, Lina M. Seo, Keun Seok Abraham, Sam Norris, Jacqueline M. Schmidt, Tracy Ehlers, Marthie M. Sordelli, Daniel O. Buzzola, Fernanda R. Gebreyes, Wondwossen A. Gonçalves, Juliano L. dos Santos, Marcos V. Zakaria, Zunita Rall, Vera L.M. [UNESP] Keane, Orla M. Niedziela, Dagmara A. Paterson, Gavin K. Holmes, Mark A. Freeman, Tom C. Fitzgerald, J. Ross |
dc.subject.por.fl_str_mv |
agriculture host adaptation phylodynamics population genomics Staphylococcus aureus |
topic |
agriculture host adaptation phylodynamics population genomics Staphylococcus aureus |
description |
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. |
publishDate |
2022 |
dc.date.none.fl_str_mv |
2022-12-13 2023-07-29T13:31:36Z 2023-07-29T13:31:36Z |
dc.type.status.fl_str_mv |
info:eu-repo/semantics/publishedVersion |
dc.type.driver.fl_str_mv |
info:eu-repo/semantics/article |
format |
article |
status_str |
publishedVersion |
dc.identifier.uri.fl_str_mv |
http://dx.doi.org/10.1073/pnas.2211217119 Proceedings of the National Academy of Sciences of the United States of America, v. 119, n. 50, 2022. 1091-6490 0027-8424 http://hdl.handle.net/11449/247996 10.1073/pnas.2211217119 2-s2.0-85143447921 |
url |
http://dx.doi.org/10.1073/pnas.2211217119 http://hdl.handle.net/11449/247996 |
identifier_str_mv |
Proceedings of the National Academy of Sciences of the United States of America, v. 119, n. 50, 2022. 1091-6490 0027-8424 10.1073/pnas.2211217119 2-s2.0-85143447921 |
dc.language.iso.fl_str_mv |
eng |
language |
eng |
dc.relation.none.fl_str_mv |
Proceedings of the National Academy of Sciences of the United States of America |
dc.rights.driver.fl_str_mv |
info:eu-repo/semantics/openAccess |
eu_rights_str_mv |
openAccess |
dc.source.none.fl_str_mv |
Scopus reponame:Repositório Institucional da UNESP instname:Universidade Estadual Paulista (UNESP) instacron:UNESP |
instname_str |
Universidade Estadual Paulista (UNESP) |
instacron_str |
UNESP |
institution |
UNESP |
reponame_str |
Repositório Institucional da UNESP |
collection |
Repositório Institucional da UNESP |
repository.name.fl_str_mv |
Repositório Institucional da UNESP - Universidade Estadual Paulista (UNESP) |
repository.mail.fl_str_mv |
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1808129265107992576 |