Abstract
Yersinia ruckeri is the causative agent of enteric redmouth disease (ERM), a serious infection that affects global aquaculture with high economic impact. The present study used whole genome sequences to perform a comparative analysis on 10 Y. ruckeri strains and to explore their genetic relatedness to other members of the genus. Y. ruckeri, Yersinia entomophaga, and Yersinia nurmii formed a species complex that constitutes the most basal lineage of the genus. The results showed that the taxonomy of Y. ruckeri strains is better defined by using a core genome alignment and phylogenetic analysis. The distribution of accessory genes in all Yersinia species revealed the presence of 303 distinctive genes in Y. ruckeri. Of these, 169 genes were distributed in 17 genomic islands potentially involved in the pathogenesis of ERM via (1) encoding virulence factors such as Afp18, Yrp1, phage proteins and (2) improving the metabolic capabilities by enhancing utilization and metabolism of iron, amino acids (specifically, arginine and histidine), and carbohydrates. The genome of Y. ruckeri is highly conserved regarding gene structure, gene layout and functional categorization of genes. It contains various components of mobile genetic elements but lacks the CRISPR-Cas system and possesses a stable set of virulence genes possibly playing a critical role in pathogenicity. Distinct virulence plasmids were exclusively restricted to a specific clonal group of Y. ruckeri (CG4), possibly indicating a selective advantage. Phylogenetic analysis of Y. ruckeri genomes revealed the co-presence of multiple genetically distant lineages of Y. ruckeri strains circulating in Germany. Our results also suggest a possible dissemination of a specific group of strains in the United States, Peru, Germany, and Denmark. In conclusion, this study provides new insights into the taxonomy and evolution of Y. ruckeri and contributes to a better understanding of the pathogenicity of ERM in aquaculture. The genomic analysis presented here offers a framework for the development of more efficient control strategies for this pathogen.
Highlights
RESULTSThe genus Yersinia currently comprises 26 species with different ecological habitats and pathogenicity
In this study, (1) we describe the genomic features of ten circularized genomes of Y. ruckeri strains of mostly clinical origin; (2) explore the genetic relatedness of Y. ruckeri within the genus Yersinia by comparing our data with the genomic data of 90 representative strains of all validly published Yersinia species; (3) describe the comparative phylogenetic analysis and in silico virulence profiling of the ten sequenced strains with published genomes of 67 Y. ruckeri strains
Our results show that the genetic relatedness of the species is better delineated using core genome alignment followed by phylogenetic analysis rather than genome-wide allele typing or 16S rRNA gene analysis
Summary
RESULTSThe genus Yersinia currently comprises 26 species with different ecological habitats and pathogenicity. Strains can be distinguished according to their biotypes (biotype 1 and biotype 2), serotypes (O1a, b; O2 a, b, c; O3; and O4) as well as their outer membrane protein (OMP) profiles (Romalde and Toranzo, 1993; Kumar et al, 2015; Wrobel et al, 2020). OMPs contribute significantly to the composition of the outer membrane of Gram-negative bacteria and play a major role in virulence. Studies on the composition of the outer membrane proteome of Y. ruckeri isolates from rainbow trout and Atlantic salmon revealed a high degree of variation between strains (Ormsby et al, 2019; Ormsby and Davies, 2021). The current knowledge on virulence factors and infection pathways of Y. ruckeri is outlined in recently published reviews (Guijarro et al, 2018; Wrobel et al, 2019)
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