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.

The Yersinia pseudotuberculosis complex: characterization and delineation of a new species, Yersinia wautersii.

The genus Yersinia contains three species pathogenic for humans, one of which is the enteropathogen Yersinia pseudotuberculosis. A recent analysis by Multi Locus Sequence Typing (MLST) of the 'Y. pseudotuberculosis complex' revealed that this complex comprises three distinct populations: the Y. pestis/Y. pseudotuberculosis group, the recently described species Yersinia similis, and a third not yet characterized population designated 'Korean Group', because most strains were isolated in Korea. The aim of this study was to perform an in depth phenotypic and genetic characterization of the three populations composing the Y. pseudotuberculosis complex (excluding Y. pestis, which belonged to the Y. pseudotuberculosis cluster in the MLST analysis). Using a set of strains representative of each group, we found that the three populations had close metabolic properties, but were nonetheless distinguishable based on D-raffinose and D-melibiose fermentation, and on pyrazinamidase activity. Moreover, high-resolution electrospray mass spectrometry highlighted protein peaks characteristic of each population. Their 16S rRNA gene sequences shared high identity (≥99.5%), but specific nucleotide signatures for each group were identified. Multi-Locus Sequence Analysis also identified three genetically closely related but distinct populations. Finally, an Average Nucleotide Identity (ANI) analysis performed after sequencing the genomes of a subset of strains of each group also showed that intragroup identity (average for each group ≥99%) was higher than intergroup diversity (94.6-97.4%). Therefore, all phenotypic and genotypic traits studied concurred with the initial MLST data indicating that the Y. pseudotuberculosis complex comprises a third and clearly distinct population of strains forming a novel Yersinia species that we propose to designate Yersinia wautersii sp. nov. The isolation of some strains from humans, the detection of virulence genes (on the pYV and pVM82 plasmids, or encoding the superantigen ypmA) in some isolates, and the absence of pyrazinamidase activity (a hallmark of pathogenicity in the genus Yersinia) argue for the pathogenic potential of Y. wautersii.

Characterization of atypical isolates of Yersinia intermedia and definition of two new biotypes.

The species Yersinia intermedia is a member of the genus Yersinia which belongs to the Enterobacteriaceae family. This species is divided into eight biotypes, according to Brenner's biotyping scheme. This scheme relies on five tests (utilization of Simmons citrate and acid production from d-melibiose, d-raffinose, alpha-methyl-d-glucoside [alphaMG], and l-rhamnose). The collection of the French Yersinia Reference Laboratory (Institut Pasteur, Paris, France) contained 44 strains that were originally identified as Y. intermedia but whose characteristics did not fit into the biotyping scheme. These 44 strains were separated into two biochemical groups: variant 1 (positive for acid production from l-rhamnose and alphaMG and positive for Simmons citrate utlization) and variant 2 (positive for acid production from l-rhamnose and alphaMG). These atypical strains could correspond to new biotypes of Y. intermedia, to Y. frederiksenii strains having the atypical property of fermenting alphaMG, or to new Yersinia species. These strains did not exhibit growth or phenotypic properties different from those of Y. intermedia and Y. frederiksenii and did not harbor any of the virulence traits usually found in pathogenic species. DNA-DNA hybridizations performed between one strain each of variants 1 and 2 and the Y. intermedia and Y. frederiksenii type strains demonstrated that these variants do belong to the Y. intermedia species. We thus propose that Brenner's biotyping scheme be updated by adding two new biotypes: 9 (for variant 1) and 10 (for variant 2) to the species Y. intermedia.

Sudden onset of pseudotuberculosis in humans, France, 2004-05.

Cases of Yersinia pseudotuberculosis infection increased in France during the winter of 2004-05 in the absence of epidemiologic links between patients or strains. This increase represents transient amplification of a pathogen endemic to the area and may be related to increased prevalence of the pathogen in rodent reservoirs.

Yersiniosis in France: overview and potential sources of infection.

OBJECTIVES: The aim of this study was to exploit the extensive database on strains of Yersinia collected over more than 50 years in France in order to gain an overview of yersiniosis and potential sources of contamination in this country. METHODS: The 19 670 strains of Yersinia of human, animal, environmental, and food origin isolated in France were grouped by species, biotype, and serotype. RESULTS: Most human strains (59%) were pathogenic, with a marked predominance of Yersinia enterocolitica bioserotype 4/O:3 (66.8%), followed by Y. enterocolitica 2/O:9 (23.8%) and Yersinia pseudotuberculosis (6.1%). Pigs and pork meat were the nearly exclusive sources of Y. enterocolitica 4/O:3. Other pathogenic strains were rarely isolated from food or environmental samples (0.2%). The major source of pathogenic Yersinia was the animal reservoir, with a remarkable association between Y. enterocolitica 4/O:3 and pigs, Y. pseudotuberculosis and wildlife, Y. enterocolitica 2/O:9 and grazing farm animals, Y. enterocolitica 5/O:2,3 and hares, and Y. enterocolitica 3/O:1,2,3 and chinchillas. CONCLUSIONS: The frequency of human infection caused by certain Yersinia subgroups might be related to the frequency of exposure to specific animal sources. In contrast, non-pathogenic Yersinia were commonly isolated from foodstuffs and the environment, most probably accounting for the abundance of non-pathogenic Yersinia recovered from human stools.

Investigation of an unusual increase in human yersinioses in Creuse, France.

OBJECTIVES: To investigate an unusual cluster of Y. enterocolitica 4/O:3/VIII human infections that occurred in Creuse (France) during the summer 2008, and to perform retrospective and prospective analyses of yersiniosis cases to get a better view of the general trend. METHODS: 33 pathogenic Y. enterocolitica strains isolated between 2008 and 2010 in Creuse were subjected to phenotypic and molecular typing. The database of the Yersinia National Reference Laboratory was used to compare the number of human cases over 23 years in Creuse and at the national level. RESULTS: The 33 isolates had three distinct phenotypes and a high genetic diversity, ruling out a unique source of contamination. A long-term analysis of yersiniosis cases in Creuse showed a progressive increase over years, with a peak in 2008 and a subsequent decrease. This trend contrasted with the national cases that showed an opposite pattern. CONCLUSIONS: Local environmental conditions were most likely responsible for a transient expansion of pathogenic Y. enterocolitica strains in Creuse.

Fatal Yersinia enterocolitica biotype 4 serovar O:3 sepsis after red blood cell transfusion.

BACKGROUND: Although posttransfusion bacterial sepsis is rare, this complication is associated with a high mortality rate. CASE REPORT: A fatal case of septic shock was observed in a 71-year-old patient following transfusion of contaminated red blood cells (RBCs) for refractory anemia. Yersinia enterocolitica was isolated from the patient's blood sample and the transfused RBCs. Both strains were of bioserotype 4/O:3 and had the same NotI pulsotype. High titers of antibodies against Y. enterocolitica were detected in the donor's plasma sample 1 month after blood donation. The donor reported abdominal discomfort 3.5 months before blood collection but had no clinical signs of intestinal infection at the time of donation. CONCLUSION: Y. enterocolitica has been identified with increased frequency as a causative agent of posttransfusion septic shock. This nationwide investigation of these cases led to an estimated incidence of one case per 6.5 million RBC units distributed in France. Although rare, this often fatal complication remains nonpreventable worldwide owing to the lack of practical means for screening RBCs before transfusion.