Investigation of the genus Flavobacterium as a reservoir for fish-pathogenic bacterial species: the case of Flavobacterium collinsii

Bacteria of the genus Flavobacterium are recovered from a large variety of environments. Among the described species, Flavobacterium psychrophilum and Flavobacterium columnare are causing considerable losses in fish farms. Alongside these well-known fish-pathogenic species, isolates belonging to the same genus recovered from diseased or apparently healthy wild, feral, and farmed fish have been suspected to be pathogenic. Here, we report the identification and genomic characterization of a F. collinsii isolate (TRV642) retrieved from rainbow trout spleen. A phylogenetic tree of the genus built by aligning the core genome of 195 Flavobacterium species revealed that F. collinsii is standing within a cluster of species associated to diseased fish, the closest one being F. tructae which was recently confirmed as pathogenic. We evaluated the pathogenicity of F. collinsii TRV642 as well as of F. bernardetii F-372T, another recently described species reported as a possible emerging pathogen. Following intramuscular injection challenges in rainbow trout, no clinical signs nor mortalities were observed. However, F. collinsii was isolated from the internal organs of wounded fish, suggesting that the bacterium could invade fish under compromised conditions such as stress and/or wounds. Our results suggest that some fish-associated Flavobacterium species should be considered as opportunistic fish pathogens causing disease under specific circumstances. IMPORTANCEAquaculture has expanded significantly worldwide in the last decades and accounts for half of human fish consumption. However, infectious fish diseases are a major bottleneck for its sustainable development and an increasing number of bacterial species from diseased fish raise a great concern. The current study revealed phylogenetic associations with ecological niches among the Flavobacterium species. We also focused on Flavobacterium collinsii that belongs to a group of putative pathogenic species. The genome contents revealed a versatile metabolic repertoire suggesting the use of diverse nutrient sources, a characteristic of saprophytic or commensal bacteria. In a rainbow trout experimental challenge, the bacterium colonized only oppressed fish facing stressful conditions suggesting opportunistic pathogenic behavior. This study highlights the importance of experimentally evaluating the pathogenicity of the numerous bacterial species retrieved from diseased fish.