Evidence for common ancestry and microevolution of passerine-adapted Salmonella enterica serovar Typhimurium in the UK and USA

Abstract

The evolution of Salmonella enterica serovar Typhimurium (S. Typhimurium) within passerines has resulted in pathoadaptation of this serovar to the avian host in Europe. Recently, we identified an S. Typhimurium lineage from passerines in North America. The emergence of passerine-adapted S. Typhimurium in Europe and North America raises questions regarding its evolutionary origin. Here, we demonstrated that the UK and US passerine-adapted S. Typhimurium shared a common ancestor from ca. 1838, and larids played a key role in the clonal expansion by disseminating the common ancestor between North America and Europe. Further, we identified virulence gene signatures common in the passerine- and larid-adapted S. Typhimurium, including conserved pseudogenes in fimbrial gene lpfD and Type 3 Secretion System (T3SS) effector gene steC. However, the UK and US passerine-adapted S. Typhimurium also possessed unique virulence gene signatures (i.e. pseudogenes in fimbrial gene fimC and T3SS effector genes sspH2, gogB, sseJ and sseK2), and the majority of them (38/47) lost a virulence plasmid pSLT that was present in the larid-adapted S. Typhimurium. These results provide evidence that passerine-adapted S. Typhimurium share a common ancestor with those from larids, and the divergence of passerine- and larid-adapted S. Typhimurium might be due to pseudogenization or loss of specific virulence genes.