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Abstract

Epidemic and pandemic clones of bacterial pathogens with distinct characteristics continually emerge, replacing those previously dominant through mechanisms that remain poorly characterized. Here, whole-genome-sequencing-powered epidemiology linked horizontal transfer of a virulence gene, , to the emergence and clonal expansion of a new epidemic serovar Typhimurium (. Typhimurium) clone. The gene is sporadically distributed within the genus and rare in . Typhimurium lineages, but was acquired multiple times during clonal expansion of the currently dominant pandemic monophasic . Typhimurium sequence type (ST) 34 clone. Ancestral state reconstruction and time-scaled phylogenetic analysis indicated that was not present in the common ancestor of the epidemic clade, but later acquisition resulted in increased clonal expansion of -containing clones that was temporally associated with emergence of the epidemic, consistent with increased fitness. The gene was mainly associated with a temperate bacteriophage mTmV, but recombination with other bacteriophage and apparent horizontal gene transfer of the gene cassette resulted in distribution among at least four mobile genetic elements within the monophasic . Typhimurium ST34 epidemic clade. The mTmV prophage lysogenic transfer to other serovars was limited, but included the common pig-associated . Derby (. Derby). This may explain mTmV in . Derby co-circulating on farms with monophasic . Typhimurium ST34, highlighting the potential for further transfer of the virulence gene in nature. We conclude that whole-genome epidemiology pinpoints potential drivers of evolutionary and epidemiological dynamics during pathogen emergence, and identifies targets for subsequent research in epidemiology and bacterial pathogenesis.

Funding
This study was supported by the:
  • Teagasc, http://dx.doi.org/10.13039/501100001604 (Award 2015028)
  • Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268 (Award BB/R012504/1)
  • Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268 (Award BB/M025489/1)
  • Biotechnology and Biological Sciences Research Council, http://dx.doi.org/10.13039/501100000268 (Award BB/N007964/1)
  • This is an open-access article distributed under the terms of the Creative Commons Attribution License.
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2020-10-28
2024-03-28
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