The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs
Murray, Gemma G. R. (University of Cambridge. Department of Veterinary Medicine)
Hossain, A. S. Md. Mukarram (Cancer Research UK Manchester Institute)
Miller, Eric L. (Haverford College. Department of Biology)
Bruchmann, Sebastian (University of Cambridge. Department of Veterinary Medicine)
Balmer, Andrew J. (University of Cambridge. Department of Veterinary Medicine)
Matuszewska, Marta (University of Cambridge. Department of Veterinary Medicine)
Herbert, Josephine (University of Portsmouth. Centre for Enzyme Innovation)
Hadjirin, Nazreen F. (University of Oxford. Nuffield Department of Population Health)
Mugabi, Robert (Iowa State University. College of Veterinary Medicine)
Li, Ganwu (Iowa State University. College of Veterinary Medicine)
Ferrando, Maria Laura (Wageningen University. Animal Sciences Department)
Fernandes de Oliveira, Isabela Maria (Wageningen University. Animal Sciences Department)
Nguyen, Thanh (Oxford University Clinical Research Unit)
Yen, Phung L. K. (Oxford University Clinical Research Unit)
Phuc, Ho D. (Oxford University Clinical Research Unit)
Zaw Moe, Aung (Livestock Breeding and Veterinary Department)
Su Wai, Thiri (Livestock Breeding and Veterinary Department)
Gottschalk, Marcelo (University of Montreal)
Aragon, Virginia (Unitat mixta d'investigació IRTA-UAB en Sanitat Animal. Centre de Recerca en Sanitat Animal)
Valentin-Weigand, Peter (University of Veterinary Medicine Hannover. Institute for Microbiology)
Heegaard, Peter M. H. (Technical University of Denmark. Department of Health Technology)
Vrieling, Manouk (Wageningen Bioveterinary Research)
Thein Maw, Min (Livestock Breeding and Veterinary Department)
Thidar Myint, Hnin (Livestock Breeding and Veterinary Department)
Tun Win, Ye (Livestock Breeding and Veterinary Department)
Thi Hoa, Ngo (Ngoc Thach University of Medicine. Microbiology Department and Center for Tropical Medicine Research)
Bentley, Stephen D. (Wellcome Sanger Institute. Parasites and Microbes Programme)
Clavijo, Maria J. (Iowa State University. College of Veterinary Medicine)
Wells, Jerry M. (Wageningen University. Animal Sciences Department)
Tucker, Alexander W. (University of Cambridge. Department of Veterinary Medicine)
Weinert, Lucy A. (University of Cambridge. Department of Veterinary Medicine)

Data:	2023
Resum:	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.
Ajuts:	European Commission. Horizon 2020 727966
Nota:	Altres ajuts: Biotechnology and Biological Sciences Research Council BB/L018934/1. Wellcome Trust and Royal Society 109385/Z/15/Z. Medical Research Council MR/V032836/1 i Royal Society CH16011
Drets:	Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.
Llengua:	Anglès
Document:	Article ; recerca ; Versió publicada
Matèria:	Streptococcus suis ; Pathogen emergence ; Bacterial pathogens ; Comparative genomics ; Livestock pathogens
Publicat a:	Proceedings of the National Academy of Sciences of the United States of America, Vol. 120 (november 2023) , ISSN 1091-6490

DOI: 10.1073/pnas.2307773120
PMID: 37963246

11 p, 3.5 MB

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