The emergence and diversification of a zoonotic pathogen from within the microbiota of intensively farmed pigs

Gemma G R Murray, A S Md Mukarram Hossain, Eric L Miller, Sebastian Bruchmann, Andrew J Balmer, Marta Matuszewska, Josephine Herbert, Nazreen F Hadjirin, Robert Mugabi, Ganwu Li, Maria Laura Ferrando, Isabela Maria Fernandes de Oliveira, Thanh Nguyen, Phung L K Yen, Ho D Phuc, Aung Zaw Moe, Thiri Su Wai, Marcelo Gottschalk, Virginia Aragon, Peter Valentin-WeigandPeter M H Heegaard, Manouk Vrieling, Min Thein Maw, Hnin Thidar Myint, Ye Tun Win, Ngo Thi Hoa, Stephen D Bentley, Maria J Clavijo, Jerry M Wells, Alexander W Tucker, Lucy A Weinert

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Abstract

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.

Original languageEnglish
Article numbere2307773120
Number of pages11
JournalProceedings of the National Academy of Sciences of the United States of America
Volume120
Issue number47
DOIs
Publication statusPublished - 14 Nov 2023

Keywords

  • Streptococcus suis
  • pathogen emergence
  • bacterial pathogens
  • comparative genomic
  • livestock pathogens
  • UKRI
  • MRC
  • MR/V032836/1

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