The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs
There is growing concern that rapid growth in livestock production and major changes in farming practices are driving the emergence of pathogens capable of causing disease in both livestock and humans. However, most studies neglect livestock microbiota as a potential source of emerging pathogens. He...
| Autores: | ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; ; |
|---|---|
| Tipo de documento: | Artículo |
| Fecha de publicación: | 2023 |
| País: | España |
| Institución: | Universitat Autònoma de Barcelona |
| Repositorio: | Dipòsit Digital de Documents de la UAB |
| Lenguaje: | Inglés |
| OAI Identifier: | oai:ddd.uab.cat:289722 |
| Acceso en línea: | https://ddd.uab.cat/record/289722 https://dx.doi.org/urn:doi:10.1073/pnas.2307773120 |
| Nivel de acceso: | Acceso abierto |
| Palabra clave: | Streptococcus suis Pathogen emergence Bacterial pathogens Comparative genomics Livestock pathogens |
| _version_ | 1878739747183001600 |
|---|---|
| author | Murray, Gemma G. R.|||0000-0002-9531-1711 |
| author2 | Hossain, A. S. Md. Mukarram|||0000-0003-2654-8982 Miller, Eric L. Bruchmann, Sebastian|||0000-0001-8721-5386 Balmer, Andrew J. Matuszewska, Marta|||0000-0002-2653-7725 Herbert, Josephine|||0000-0002-8352-6344 Hadjirin, Nazreen F. Mugabi, Robert|||0000-0001-8919-059X Li, Ganwu|||0000-0002-6370-9573 Ferrando, Maria Laura|||0000-0002-1398-8244 Fernandes de Oliveira, Isabela Maria Nguyen, Thanh|||0000-0002-8541-5023 Yen, Phung L. K. Phuc, Ho D. Zaw Moe, Aung Su Wai, Thiri Gottschalk, Marcelo|||0000-0002-2196-2212 Aragón, Virginia|||0000-0002-3470-6015 Valentin-Weigand, Peter Heegaard, Peter M. H.|||0000-0003-4506-4932 Vrieling, Manouk Thein Maw, Min Thidar Myint, Hnin Tun Win, Ye Thi Hoa, Ngo Bentley, Stephen D.|||0000-0001-8094-3751 Clavijo, Maria J. Wells, Jerry M. Tucker, Alexander W. Weinert, Lucy A. |
| 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 author author author author author author author |
| author_browse | Aragón, Virginia|||0000-0002-3470-6015 Balmer, Andrew J. Bentley, Stephen D.|||0000-0001-8094-3751 Bruchmann, Sebastian|||0000-0001-8721-5386 Clavijo, Maria J. Fernandes de Oliveira, Isabela Maria Ferrando, Maria Laura|||0000-0002-1398-8244 Gottschalk, Marcelo|||0000-0002-2196-2212 Hadjirin, Nazreen F. Heegaard, Peter M. H.|||0000-0003-4506-4932 Herbert, Josephine|||0000-0002-8352-6344 Hossain, A. S. Md. Mukarram|||0000-0003-2654-8982 Li, Ganwu|||0000-0002-6370-9573 Matuszewska, Marta|||0000-0002-2653-7725 Miller, Eric L. Mugabi, Robert|||0000-0001-8919-059X Murray, Gemma G. R.|||0000-0002-9531-1711 Nguyen, Thanh|||0000-0002-8541-5023 Phuc, Ho D. Su Wai, Thiri Thein Maw, Min Thi Hoa, Ngo Thidar Myint, Hnin Tucker, Alexander W. Tun Win, Ye Valentin-Weigand, Peter Vrieling, Manouk Weinert, Lucy A. Wells, Jerry M. Yen, Phung L. K. Zaw Moe, Aung |
| author_facet | Murray, Gemma G. R.|||0000-0002-9531-1711 Hossain, A. S. Md. Mukarram|||0000-0003-2654-8982 Miller, Eric L. Bruchmann, Sebastian|||0000-0001-8721-5386 Balmer, Andrew J. Matuszewska, Marta|||0000-0002-2653-7725 Herbert, Josephine|||0000-0002-8352-6344 Hadjirin, Nazreen F. Mugabi, Robert|||0000-0001-8919-059X Li, Ganwu|||0000-0002-6370-9573 Ferrando, Maria Laura|||0000-0002-1398-8244 Fernandes de Oliveira, Isabela Maria Nguyen, Thanh|||0000-0002-8541-5023 Yen, Phung L. K. Phuc, Ho D. Zaw Moe, Aung Su Wai, Thiri Gottschalk, Marcelo|||0000-0002-2196-2212 Aragón, Virginia|||0000-0002-3470-6015 Valentin-Weigand, Peter Heegaard, Peter M. H.|||0000-0003-4506-4932 Vrieling, Manouk Thein Maw, Min Thidar Myint, Hnin Tun Win, Ye Thi Hoa, Ngo Bentley, Stephen D.|||0000-0001-8094-3751 Clavijo, Maria J. Wells, Jerry M. Tucker, Alexander W. Weinert, Lucy A. |
| author_role | author |
| collection | Dipòsit Digital de Documents de la UAB |
| description | There is growing concern that rapid growth in livestock production and major changes in farming practices are driving the emergence of pathogens capable of causing disease in both livestock and humans. However, most studies neglect livestock microbiota as a potential source of emerging pathogens. Here, we show how the global transport of live animals has facilitated the emergence of an important livestock and human zoonotic pathogen from a common member of the pig respiratory microbiota. Our results indicate that pathogenic lineages are likely to continue to emerge and diversify and recommend ways of controlling this. The expansion and intensification of livestock production is predicted to promote the emergence of pathogens. As pathogens sometimes jump between species, this can affect the health of humans as well as livestock. Here, we investigate how livestock microbiota can act as a source of these emerging pathogens through analysis of Streptococcus suis, a ubiquitous component of the respiratory microbiota of pigs that is also a major cause of disease on pig farms and an important zoonotic pathogen. Combining molecular dating, phylogeography, and comparative genomic analyses of a large collection of isolates, we find that several pathogenic lineages of S. suis emerged in the 19th and 20th centuries, during an early period of growth in pig farming. These lineages have since spread between countries and continents, mirroring trade in live pigs. They are distinguished by the presence of three genomic islands with putative roles in metabolism and cell adhesion, and an ongoing reduction in genome size, which may reflect their recent shift to a more pathogenic ecology. Reconstructions of the evolutionary histories of these islands reveal constraints on pathogen emergence that could inform control strategies, with pathogenic lineages consistently emerging from one subpopulation of S. suis and acquiring genes through horizontal transfer from other pathogenic lineages. These results shed light on the capacity of the microbiota to rapidly evolve to exploit changes in their host population and suggest that the impact of changes in farming on the pathogenicity and zoonotic potential of S. suis is yet to be fully realized. |
| eu_rights_str_mv | openAccess |
| format | article |
| id | ES_c73f649e4e79aebae9cfb519cd6ca9f6 |
| institution | Universitat Autònoma de Barcelona |
| instname_str | Universitat Autònoma de Barcelona |
| language | eng |
| network_acronym_str | ES |
| network_name_str | España |
| oai_identifier_str | oai:ddd.uab.cat:289722 |
| publishDate | 2023 |
| publishDateSort | 2023 |
| reponame_str | Dipòsit Digital de Documents de la UAB |
| spelling | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs Murray, Gemma G. R.|||0000-0002-9531-1711 Hossain, A. S. Md. Mukarram|||0000-0003-2654-8982 Miller, Eric L. Bruchmann, Sebastian|||0000-0001-8721-5386 Balmer, Andrew J. Matuszewska, Marta|||0000-0002-2653-7725 Herbert, Josephine|||0000-0002-8352-6344 Hadjirin, Nazreen F. Mugabi, Robert|||0000-0001-8919-059X Li, Ganwu|||0000-0002-6370-9573 Ferrando, Maria Laura|||0000-0002-1398-8244 Fernandes de Oliveira, Isabela Maria Nguyen, Thanh|||0000-0002-8541-5023 Yen, Phung L. K. Phuc, Ho D. Zaw Moe, Aung Su Wai, Thiri Gottschalk, Marcelo|||0000-0002-2196-2212 Aragón, Virginia|||0000-0002-3470-6015 Valentin-Weigand, Peter Heegaard, Peter M. H.|||0000-0003-4506-4932 Vrieling, Manouk Thein Maw, Min Thidar Myint, Hnin Tun Win, Ye Thi Hoa, Ngo Bentley, Stephen D.|||0000-0001-8094-3751 Clavijo, Maria J. Wells, Jerry M. Tucker, Alexander W. Weinert, Lucy A. Streptococcus suis Pathogen emergence Bacterial pathogens Comparative genomics Livestock pathogens There is growing concern that rapid growth in livestock production and major changes in farming practices are driving the emergence of pathogens capable of causing disease in both livestock and humans. However, most studies neglect livestock microbiota as a potential source of emerging pathogens. Here, we show how the global transport of live animals has facilitated the emergence of an important livestock and human zoonotic pathogen from a common member of the pig respiratory microbiota. Our results indicate that pathogenic lineages are likely to continue to emerge and diversify and recommend ways of controlling this. The expansion and intensification of livestock production is predicted to promote the emergence of pathogens. As pathogens sometimes jump between species, this can affect the health of humans as well as livestock. Here, we investigate how livestock microbiota can act as a source of these emerging pathogens through analysis of Streptococcus suis, a ubiquitous component of the respiratory microbiota of pigs that is also a major cause of disease on pig farms and an important zoonotic pathogen. Combining molecular dating, phylogeography, and comparative genomic analyses of a large collection of isolates, we find that several pathogenic lineages of S. suis emerged in the 19th and 20th centuries, during an early period of growth in pig farming. These lineages have since spread between countries and continents, mirroring trade in live pigs. They are distinguished by the presence of three genomic islands with putative roles in metabolism and cell adhesion, and an ongoing reduction in genome size, which may reflect their recent shift to a more pathogenic ecology. Reconstructions of the evolutionary histories of these islands reveal constraints on pathogen emergence that could inform control strategies, with pathogenic lineages consistently emerging from one subpopulation of S. suis and acquiring genes through horizontal transfer from other pathogenic lineages. These results shed light on the capacity of the microbiota to rapidly evolve to exploit changes in their host population and suggest that the impact of changes in farming on the pathogenicity and zoonotic potential of S. suis is yet to be fully realized. https://ddd.uab.cat/record/289722 https://dx.doi.org/urn:doi:10.1073/pnas.2307773120 |
| spellingShingle | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs Murray, Gemma G. R.|||0000-0002-9531-1711 Streptococcus suis Pathogen emergence Bacterial pathogens Comparative genomics Livestock pathogens |
| title | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| title_full | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| title_fullStr | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| title_full_unstemmed | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| title_short | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| title_sort | The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs |
| topic | Streptococcus suis Pathogen emergence Bacterial pathogens Comparative genomics Livestock pathogens |
| topic_facet | Streptococcus suis Pathogen emergence Bacterial pathogens Comparative genomics Livestock pathogens |
| url | https://ddd.uab.cat/record/289722 https://dx.doi.org/urn:doi:10.1073/pnas.2307773120 |