Genomic Diversity and Evolution of the Fish Pathogen Flavobacterium psychrophilum

Abstract

Flavobacterium psychrophilum, the etiological agent of rainbow trout fry syndrome and bacterial cold-water disease in salmonid fish, is currently one of the main bacterial pathogens hampering the productivity of salmonid farming worldwide. In this study, the genomic diversity of the F. psychrophilum species is analyzed using a set of 41 genomes, including 30 newly sequenced isolates. These were selected on the basis of available MLST data with the two-fold objective of maximizing the coverage of the species diversity and of allowing a focus on the main clonal complex (CC-ST10) infecting farmed rainbow trout (Oncorhynchus mykiss) worldwide. The results reveal a bacterial species harboring a limited genomic diversity both in terms of nucleotide diversity, with ~0.3% nucleotide divergence inside CDSs in pairwise genome comparisons, and in terms of gene repertoire, with the core genome accounting for ~80% of the genes in each genome. The pan-genome seems nevertheless “open” according to the scaling exponent of a power-law fitted on the rate of new gene discovery when genomes are added one-by-one. Recombination is a key component of the evolutionary process of the species as seen in the high level of apparent homoplasy in the core genome. Using a Hidden Markov Model to delineate recombination tracts in pairs of closely related genomes, the average recombination tract length was estimated to ~4.0 Kbp and the typical ratio of the contributions of recombination and mutations to nucleotide-level differentiation (r/m) was estimated to ~13. Within CC-ST10, evolutionary distances computed on non-recombined regions and comparisons between 22 isolates sampled up to 27 years apart suggest a most recent common ancestor in the second half of the nineteenth century in North America with subsequent diversification and transmission of this clonal complex coinciding with the worldwide expansion of rainbow trout farming. With the goal to promote the development of tools for the genetic manipulation of F. psychrophilum, a particular attention was also paid to plasmids. Their extraction and sequencing to completion revealed plasmid diversity that remained hidden to classical plasmid profiling due to size similarities.

Large-Scale Analysis of Flavobacterium psychrophilum Multilocus Sequence Typing Genotypes Recovered from North American Salmonids Indicates that both Newly Identified and Recurrent Clonal Complexes Are Associated with Disease

“…Within North America, CC-ST10 was the most widespread among currently recognized CCs, being detected in 16 of the 20 states in the Northwest, West, Southwest, Midwest, Southeast, and Northeast regions of the United States that were examined in this study. This finding is consistent with other studies that have suggested that ST10, the predicted CC founder strain (12), along with other CC-ST10 STs, have been disseminated around the world as a result of the international salmonid egg trade, where they are also now widespread (13,17).…”

“…Combining data from this study with those of Nicolas et al (7) and Van Vliet et al (13) revealed that the mean gene diversity of MLST-typed F. psychrophilum in North America is higher than in all other studied continents (i.e., 0.68 in North America versus 0.48 to 0.66 elsewhere). In this context, a recent study provided evidence that the main lineage of F. psychrophilum causing disease in rainbow trout (i.e., CC-ST10) may have originated in North America, from where at least one successful genotype (e.g., ST10) was distributed to other regions of the world through the international trade of fish (17). If this F. psychrophilum lineage did indeed originate in North America, it would have had more time to diversify in this region, perhaps resulting in the high apparent genetic diversity discovered in this study.…”

Identification of Four Distinct Phylogenetic Groups in Flavobacterium columnare With Fish Host Associations

“…The use of low variation and higher variation genes likely contribute to the topology inconsistencies observed between markers. Due to the observation of variable topologies following phylogenetic analyses of different markers in the present and previous studies, future research should critically analyze whole genome sequences and construct genome based phylogenies to gain a better understanding of how these genetic groups were established as was recently published with F. psychrophilum ( Duchaud et al, 2018 ).…”

Application of Metagenomics to Chilean Aquaculture

“…In fact, using less water surface, Chile competes to Norway in salmon production [12]. As consequence, Chilean aquaculture has faced several sanitary problems, related with outbreaks of viruses such as infectious pancreatic necrosis virus (IPNV) [13] and infectious salmon anemia virus (ISAV) [14]; bacterial pathogens such as Piscirickettsia salmonis [15], Flavobacterium psychrophilum [16], and Renibacterium salmoninarum [17]; and parasites such as Caligus rogercresseyi [15]. Diseases caused by viruses are one of the great challenges of Chilean salmon farming industry; the first virus being identified in Chile was IPNV, which is highly persistent and causes severe mortality.…”