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.

The myxozoan parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) infection dynamics and host specificity in hybrid tilapia aquaculture

“…Infection rates in the fish pond labelled L peaked during August, as we observed in pond M in our previous study (Maor-Landaw et al, 2022). This result is not surprising, as many studies have linked myxozoan infection with seasonal increase in temperatures (Schmidt-Posthaus and Wahli, 2015).…”

“…In the large rearing pond, where the fish spend several months, more fish-actinospore encounters are likely to happen, which would result in increased parasite load in the fish's gills. Ultimately, an immune-compromised individual will continuously be challenged by various opportunistic pathogens (Maor-Landaw et al, 2022).…”

“…Specific qPCR primers were utilized to amplify M. bejeranoi SSU rRNA gene (NCBI accession number MF401455) (Lövy et al, 2018) and tilapia β-actin gene was used as a normalizer gene (Zhou et al, 2019) (Table S1) for the comparative ΔΔCTs method. qPCR was performed on 25 ng DNA as previously described (Maor-Landaw et al, 2022) and normalized expression levels were calculated.…”

“…Myxozoan parasites cause morbidity and mortality, such as whirling disease and proliferative kidney disease, in both farmed and wild fish populations worldwide (Okamura et al, 2015). Recently, the causative agent of hybrid tilapia infections, which occur at more than 50% prevalence during the summer season in commercial fish ponds (Maor-Landaw et al, 2022), was classified as Myxobolus bejeranoi (Lövy et al, 2018). The infection is limited to the gills, where cysts are formed on striated muscle of the gill filament base (Lövy et al, 2018).…”

“…The infection is limited to the gills, where cysts are formed on striated muscle of the gill filament base (Lövy et al, 2018). Nevertheless, we showed recently that the effects are systemic, as inhibition of the haematopoietic organs such as head, kidney and spleen results in immune suppression and high mortality (Maor-Landaw et al, 2022). Thus, M. bejeranoi infection of hybrid tilapia has high economic impact on commercial fish farms.…”