Parallel independent evolution of pathogenicity within the genus Yersinia.

The genus Yersinia has been used as a model system to study pathogen evolution. Using whole-genome sequencing of all Yersinia species, we delineate the gene complement of the whole genus and define patterns of virulence evolution. Multiple distinct ecological specializations appear to have split pathogenic strains from environmental, nonpathogenic lineages. This split demonstrates that contrary to hypotheses that all pathogenic Yersinia species share a recent common pathogenic ancestor, they have evolved independently but followed parallel evolutionary paths in acquiring the same virulence determinants as well as becoming progressively more limited metabolically. Shared virulence determinants are limited to the virulence plasmid pYV and the attachment invasion locus ail. These acquisitions, together with genomic variations in metabolic pathways, have resulted in the parallel emergence of related pathogens displaying an increasingly specialized lifestyle with a spectrum of virulence potential, an emerging theme in the evolution of other important human pathogens.

Use of whole-genus genome sequence data to develop a multilocus sequence typing tool that accurately identifies Yersinia isolates to the species and subspecies levels.

The genus Yersinia is a large and diverse bacterial genus consisting of human-pathogenic species, a fish-pathogenic species, and a large number of environmental species. Recently, the phylogenetic and population structure of the entire genus was elucidated through the genome sequence data of 241 strains encompassing every known species in the genus. Here we report the mining of this enormous data set to create a multilocus sequence typing-based scheme that can identify Yersinia strains to the species level to a level of resolution equal to that for whole-genome sequencing. Our assay is designed to be able to accurately subtype the important human-pathogenic species Yersinia enterocolitica to whole-genome resolution levels. We also report the validation of the scheme on 386 strains from reference laboratory collections across Europe. We propose that the scheme is an important molecular typing system to allow accurate and reproducible identification of Yersinia isolates to the species level, a process often inconsistent in nonspecialist laboratories. Additionally, our assay is the most phylogenetically informative typing scheme available for Y. enterocolitica.

Directional gene flow and ecological separation in Yersinia enterocolitica.

Yersinia enterocolitica is a common cause of food-borne gastroenteritis worldwide. Recent work defining the phylogeny of the genus Yersinia subdivided Y. enterocolitica into six distinct phylogroups. Here, we provide detailed analyses of the evolutionary processes leading to the emergence of these phylogroups. The dominant phylogroups isolated from human infections, PG3-5, show very little diversity at the sequence level, but do present marked patterns of gain and loss of functions, including those involved in pathogenicity and metabolism, including the acquisition of phylogroup-specific O-antigen loci. We tracked gene flow across the species in the core and accessory genome, and show that the non-pathogenic PG1 strains act as a reservoir for diversity, frequently acting as donors in recombination events. Analysis of the core and accessory genome also suggested that the different Y. enterocolitica phylogroups may be ecologically separated, in contrast to the long-held belief of common shared ecological niches across the Y. enterocolitica species.