Infection by the parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) suppresses the immune system of hybrid tilapia

Abstract Background: Tilapia is the second most cultured fish worldwide and in Israel, it constitutes 60% of total production. Recently, the myxozoan parasite Myxobolus bejeranoi was found to infect the gills of hybrid tilapia (Nile tilapia (Oreochromis niloticus) X Jordan/Blue tilapia (O. aureus)), causing high morbidity and mortality. Myxozoa (Cnidaria) is a large group of microscopic obligate endoparasites that can cause emerging diseases, affecting wild fish populations and fisheries. Here, we aimed to elucidate the cellular processes occurring in the fish host following infection by M. bejeranoi. Methods: Comparative transcriptomics was performed on fish that had been exposed to infectious fish pond water containing M. bejeranoi actinospores for 24 hours. We compared the effects of minor, intermediate, and severe infection levels on the sporulation site, namely the gills, as well as on the hematopoietic organs head kidney and spleen. Enrichment analyses for Gene Ontology and KEGG pathways were performed and gene network was generated based on Jaccard distance matrix and visualized with Cytoscape. Results: Enrichment analysis indicated immune system activation in the gills at severe infection stage. However, in the head kidney a broad immune suppression was observed, including deactivation of secreted cytokines that play important roles in immune response of fish and of a transcription factor responsible for T helper cell differentiation. Moreover, the cytotoxic effector proteins perforin and granzyme B were down-regulated in the spleen. Finally, significant up-regulation of insulin in the spleen may imply that it functions as an immunomodulatory hormone inducing systemic immune suppression. Conclusions: Our analysis illustrates the incapacity of the hybrid tilapia host to eliminate its pathogenic invader, the myxozoan M. bejeranoi. We hypothesize that the signal for immune suppression originates at the sporulation site and traverses to the hematopoietic organs. These findings suggest that M. bejeranoi is a highly efficient parasite that disables the defense mechanisms of its fish host.