| Summary: | The genus Yersinia consists of a heterogeneous collection of organisms, comprising the highly pathogenic species Yersinia pestis, enteropathogens Yersinia pseudotuberculosis and Yersinia enterocolitica as well as environmental species. The evolutionary history of Y. pestis has been well documented, but information on the evolutionary relationship between the other Yersiniae is less characterized. Y. enterocolitica is a diverse species classed into six different biotypes (BT), but only a single genome sequence for high-pathogenic BT 1B was available at the start of the project. This project looked into the dynamics shaping the pathogenic lineages in Yersinia. For each of the Y. enterocolitica BTs, a reference genome was sequenced, annotated and analysed in detail. Analysis of biochemical characteristics was carried out using a phenotypic microarray. A further 98 Y. enterocolitica, 36 Y. pseudotuberculosis/Y. pestis isolates and 81 environmental species were sequenced and analysed to investigate the evolutionary dynamics of the genus Yersinia. The Y. enterocolitica BTs form three distinct groups according to non-, low-, and high-pathogenic BT, each with a different set of accessory genes. The Y. enterocolitica core genome comprises ~3,300 CDSs. The non-pathogenic BT contains genes involved in environmental survival, whereas the high-pathogenic BT has a high-pathogenicity island and the unique Ysa type III secretion system. The low-pathogenic BTs share a second flagella cluster and an insect pathogenicity island. Apart from the virulence plasmid pYV, only 40 CDSs are shared in all pathogenic BTs including the adhesion invasion locus ail. The phenotypic microarray confirmed higher metabolic flexibility of the non-pathogenic BT, and decreased biochemical abilities in the low-pathogenic BTs, mirroring an increased number of pseudogenes. Looking at the whole genus, pathogenic lineages are visible at opposite ends of an evolutionary tree. Y. pestis has evolved out of Y. pseudotuberculosis, and both are distinct from Y. enterocolitica which developed out of the environmental Yersiniae. Fish pathogen Y. ruckeri forms a third independent pathogenic lineage. Despite the large evolutionary distance, comparing dynamics in Y. enterocolitica to Y. pestis it is clear that independent acquisition of the virulence plasmid and metabolic streamlining to specific hosts drove pathogen evolution. Whilst this has concurrently happened in Y. pestis, this development has been weighted differently in lineages of Y. enterocolitica leading to a high-pathogenic, human-adapted biotype and lowpathogenic biotypes, which can be adapted to human or animal hosts.
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