Abstract

Yersinia ruckeri is the causative agent of enteric redmouth disease (ERM) which causes economically significant losses in farmed salmonids, especially Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss, Walbaum). However, very little is known about the genetic relationships of disease-causing isolates in these two host species or about factors responsible for disease. Phylogenetic analyses of 16 representative isolates based on the nucleotide sequences of 19 housekeeping genes suggests that pathogenic Atlantic salmon and rainbow trout isolates represent distinct host-specific lineages. However, the apparent phylogenies of certain isolates has been influenced by horizontal gene transfer and recombinational exchange. Splits decomposition analysis demonstrated a net-like phylogeny based on the housekeeping genes, characteristic of recombination. Comparative analysis of the distribution of individual housekeeping gene alleles across the isolates demonstrated evidence of genomic mosaicism and recombinational exchange involving certain Atlantic salmon and rainbow trout isolates. Comparative nucleotide sequence analysis of the key outer membrane protein genes ompA and ompF revealed that the corresponding gene trees were both non-congruent with respect to the housekeeping gene phylogenies providing evidence that horizontal gene transfer has influenced the evolution of both these surface protein-encoding genes. Analysis of inferred amino acid sequence variation in OmpA identified a single variant, OmpA.1, that was present in serotype O1 and O8 isolates representing typical pathogenic strains in rainbow trout and Atlantic salmon, respectively. In particular, the sequence of surface-exposed loop 3 differed by seven amino acids to that of other Y. ruckeri isolates. These findings suggest that positive selection has likely influenced the presence of OmpA.1 in these isolates and that loop 3 may play an important role in virulence. Amino acid sequence variation of OmpF was greater than that of OmpA and was similarly restricted mainly to the surface-exposed loops. Two OmpF variants, OmpF.1 and OmpF.2, were associated with pathogenic rainbow trout and Atlantic salmon isolates, respectively. These OmpF proteins had very similar amino acid sequences suggesting that positive evolutionary pressure has also favoured the selection of these variants in pathogenic strains infecting both species.

Highlights

  • Yersinia ruckeri is the etiological agent of enteric redmouth disease (ERM) of cultured salmonids, causing significant economic losses to the fish-farming industry

  • This study aimed to elucidate the underlying genetic relatedness of a selection of Y. ruckeri isolates from Atlantic salmon and rainbow trout based on nucleotide sequence variation in 19 housekeeping genes

  • Isolates of Y. ruckeri recovered from infected Atlantic salmon and rainbow trout represent distinct phylogenetic lineages based on the concatenated sequences of 19 housekeeping genes

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Summary

Introduction

Yersinia ruckeri is the etiological agent of enteric redmouth disease (ERM) of cultured salmonids, causing significant economic losses to the fish-farming industry. First isolated in 1956 from diseased rainbow trout (Oncorhynchus mykiss, Walbaum)[1,2], Y. ruckeri has since become widely disseminated and is present w­ orldwide[3], becoming increasingly responsible for infections in Atlantic salmon (Salmo salar). This is the case in countries, such as A­ ustralia4,5, ­Chile6,7, ­Norway[8,9], and S­ cotland[10], where salmon production is of significant economic importance. Due to the presence of OmpA in such high abundance within the O­ M18, its role in host-specifity and the numerous functions elicited are not surprising

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