Abstract

Aeromonas salmonicida is a global distributed Gram-negative teleost pathogen, affecting mainly salmonids in fresh and marine environments. A. salmonicida strains are classified as typical or atypical depending on their origin of isolation and phenotype. Five subspecies have been described, where A. salmonicida subsp. salmonicida is the only typical subspecies, and the subsp. achromogenes, masoucida, smithia, and pectinolytica are considered atypical. Genomic differences between A. salmonicida subsp. salmonicida isolates and their relationship with the current classification have not been explored. Here, we sequenced and compared the complete closed genomes of four virulent strains to elucidate their molecular diversity and pathogenic evolution using the more accurate genomic information so far. Phenotypes, biochemical, and enzymatic profiles were determined. PacBio and MiSeq sequencing platforms were utilized for genome sequencing. Comparative genomics showed that atypical strains belong to the subsp. salmonicida, with 99.55% ± 0.25% identity with each other, and are closely related to typical strains. The typical strain A. salmonicida J223 is closely related to typical strains, with 99.17% identity with the A. salmonicida A449. Genomic differences between atypical and typical strains are strictly related to insertion sequences (ISs) activity. The absence and presence of genes encoding for virulence factors, transcriptional regulators, and non-coding RNAs are the most significant differences between typical and atypical strains that affect their phenotypes. Plasmidome plays an important role in A. salmonicida virulence and genome plasticity. Here, we determined that typical strains harbor a larger number of plasmids and virulence-related genes that contribute to its acute virulence. In contrast, atypical strains harbor a single, large plasmid and a smaller number of virulence genes, reflected by their less acute virulence and chronic infection. The relationship between phenotype and A. salmonicida subspecies’ taxonomy is not evident. Comparative genomic analysis based on completed genomes revealed that the subspecies classification is more of a reflection of the ecological niche occupied by bacteria than their divergences at the genomic level except for their accessory genome.

Highlights

  • Aeromonas salmonicida is one of the oldest fish pathogens known and the causative agent of furunculosis in a wide range of hosts that live in freshwater and marine systems [1,2].A. salmonicida classification is based on the origin of isolation

  • Α-hemolysin activity was observed in atypical strains at 48 h post-incubation (Figure 1C), which became more prominent at 72 h (Figure 1D)

  • Among the unique ncRNAs in the typical A. salmonicida J223, we identified a betaproteobacteria toxic small RNA. tsRNA was previously described in Burkholderia cenocepacia and Herbaspirillum seropedicae, and the evidence suggests that it could regulate gene expression by binding to the ribosome-binding sequence of the mRNA [96]

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Summary

Introduction

A. salmonicida classification is based on the origin of isolation. A. salmonicida strains isolated from salmonids are classified as “typical” and strains isolated from non-salmonid hosts or environmental samples are classified as “atypical” strains [1,2,3]. Salmonicida is the only typical subspecies, whereas the subsp. Previous classification and phylogenetic studies of A. salmonicida isolates have demonstrated that there is high genomic divergency and plasticity among subspecies [5]. This diversity is reflected in the different biochemical features, colony size, growth rate, brown pigment synthesis, hemolytic activity, and origin of host isolation [6,7,8]

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