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.This work was primarily funded by an EU Horizon 2020 grant “PIGSs” (727966) and a ZELS BBSRC award “Myanmar Pigs Partnership (MPP)” (BB/L018934/1). G.G.R.M., E.L.M., and L.A.W. were supported by a Sir Henry Dale Fellowship to L.A.W. jointly funded by the Wellcome Trust and the Royal Society (109385/Z/15/Z). N.H. was supported by a Challenge grant from the Royal Society (CH16011) and an Isaac Newton Trust Research Grant [17.24(u)]. G.G.R.M. was also supported by a Research Fellowship at Newnham College. S.B. is supported by the Medical Research Council (MR/V032836/1). PIC North America provided part of the funds for the sequencing of the isolates from the USA. A.J.B. and M.M. were funded by Medical Research Council and Biotechnology and Biological Sciences Research Council studentships respectively, and M.M. was co-funded by the Raymond and Beverly Sackler Fund. We would like to acknowledge Susanna Williamson at the APHA for providing samples, Oscar Cabezón for sampling of the wild boar population in Spain, Mark O’Dea for access to sequence data from Australian isolates, the PIGSs and MPP consortiums for providing samples and helpful discussions, Julian Parkhill and John Welch for helpful discussions, and two anonymous reviewers for their valuable suggestions for improving the manuscript. This research was funded in whole or in part by the Wellcome Trust. For the purpose of Open Access, the author has applied a CC BY public copyright license to any Author Accepted Manuscript (AAM) version arising from this submission.info:eu-repo/semantics/publishedVersio
