Genomic diversity and evolution of the fish pathogen Flavobacterium psychrophilum

Authors: DUCHAUD, ERIC - Institut National De La Recherche Agronomique (INRA); ROCHAT, TATIANA - Institut National De La Recherche Agronomique (INRA); HABIB, CHRISTOPHE - Institut National De La Recherche Agronomique (INRA); BARBIER, PAUL - Institut National De La Recherche Agronomique (INRA); LOUX, VALENTIN - Institut National De La Recherche Agronomique (INRA); GUERIN, CYPRIEN - Institut National De La Recherche Agronomique (INRA); DALSGAARD, INGER - Technical University Of Denmark; MADSEN, LONE - Technical University Of Denmark; NILSEN, HANNE - Norwegian Veterinary Institute; SUNDELL, KRISTER - Abo Akademi University; WIKLUND, TOM - Abo Akademi University; STREPPARAVA, NICOLE - Cantonal Institute Of Microbiology Icm; WAHLI, THOMAS - Institut National De La Recherche Agronomique (INRA); CABURLOTTO, GRETA - Institute Of Experimental Zooprofilattic; MANFRIN, AMEDEO - Institute Of Experimental Zooprofilattic; Wiens, Gregory - Greg; FUJIWARA-NAGATA, ERINA - Osaka Prefecture University; AVENDANO-HERRERA, RUBEN - Universidad Andres Bello (UNAB); BERNARDET, JEAN-FRANCOIS - Institut National De La Recherche Agronomique (INRA); NICOLAS, PIERRE - Institut National De La Recherche Agronomique (INRA)

Submitted to: Frontiers in Microbiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 1/22/2018
Publication Date: 2/7/2018
Citation: Duchaud, E., Rochat, T., Habib, C., Barbier, P., Loux, V., Guerin, C., Dalsgaard, I., Madsen, L., Nilsen, H., Sundell, K., Wiklund, T., Strepparava, N., Wahli, T., Caburlotto, G., Manfrin, A., Wiens, G.D., Fujiwara-Nagata, E., Avendano-Herrera, R., Bernardet, J., Nicolas, P. 2018. Genomic diversity and evolution of the fish pathogen Flavobacterium psychrophilum. Frontiers in Microbiology. 9(138). https://doi.org/10.3389/fmicb.2018.00138.
DOI: https://doi.org/10.3389/fmicb.2018.00138

Interpretive Summary: Flavobacterium psychrophilum is a common pathogen of farmed rainbow trout but the genetic diversity of the pathogen is incompletely understood. This paper represents a large multi-institutional effort to analyze genetic diversity of 30 newly sequenced and 11 previously published genomes. Half of the sequenced genomes belong to a main grouping of isolates that are particularly virulent for rainbow trout. Analysis of the genomes identified limited genetic diversity but considerable recombination between isolates. This paper will aid the development of vaccines against this important fish pathogen.

Technical 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 twofold 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 an Hidden Markov Model to delineate recombination tracts in pairs of closely related genomes, the average recombination tract length was estimated to ~3.7 Kbp and the typical ratio of the contributions of recombination and mutations to nucleotide-level differentiation (r/m) was estimated to ~13. Evolutionary distances in CC-ST10 computed on non-recombined regions and comparisons between isolates sampled up to 27 years apart suggest the most recent common ancestor occurred ~130 years ago in North America with subsequent diversification and clonal complex transmission 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.