Diversification of OmpA and OmpF of Yersinia ruckeri is independent of the underlying species phylogeny and evidence of virulence-related selection

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.

Diagnosis of bacterial fish diseases and classification of serotypes with slide agglutination method

“…Y. ruckeri outbreaks are associated with rainbow trout dominantly represented by serotype O1, whereas the predominant serotype associated with Atlantic salmon is associated with serotype O2, O5, and O8 worldwide. (Ormsby and Davies, 2021). The findings of this study indicate that serotype O1 was responsible for the majority of the ERM cases, except Y32, Y34, and Y35 did not agglutinate with serotype O1 antisera and were untypable.…”

Allelic variation of Escherichia coli outer membrane protein A: Impact on cell surface properties, stress tolerance and allele distribution

“…enterocolitica [ 79 ] and Y . ruckeri [ 80 ]. Given the difference of (I, δ) relative abundance among E .…”

“…dysenteriae having similar OmpA sequences suggests that OmpA may be horizontally transmitted. Sequence diversity of OmpA, particularly in loop 3, of Yersinia ruckeri was concluded to be independent of phylogeny [ 80 ]. This independence was interpreted as evidence of horizontal gene transfer and selective pressure on the ompA gene.…”

Phylogenetic Relatedness and Genome Structure of Yersinia ruckeri Revealed by Whole Genome Sequencing and a Comparative Analysis

“…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). Several pathogenicity factors have been implicated in the virulence of Y. ruckeri strains, including toxins, secretion systems, iron and amino acid utilization systems, lipopolysaccharides, flagella and plasmids.…”

“…This development of "vaccine breakthrough" strains necessitates the design of new and more effective vaccines based on data obtained from comparative genome studies. Moreover, these studies can elucidate how fish pathogens spread and evolve with aquaculture, help to create management strategies to improve biosecurity and ultimately significantly reduce financial losses (Ormsby and Davies, 2021;Yang et al, 2021).…”