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

Detalhes bibliográficos
Autor(a) principal: Yebra, Gonzalo
Data de Publicação: 2022
Outros Autores: 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
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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spelling 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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