Infection by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) Suppresses the Immune System of Hybrid Tilapia

Abstract

Myxozoa (Cnidaria) is a large group of microscopic obligate endoparasites that can cause emerging diseases, affecting wild fish populations and fisheries. Recently, the myxozoan Myxobolus bejeranoi was found to infect the gills of hybrid tilapia (Nile tilapia (Oreochromis niloticus) × Jordan/blue tilapia (O. aureus)), causing high morbidity and mortality. Here, we used comparative transcriptomics to elucidate the molecular processes occurring in the fish host following infection by M. bejeranoi. Fish were exposed to pond water containing actinospores for 24 h and the effects of minor, intermediate, and severe infections on the sporulation site, the gills, and on the hematopoietic organs, head kidney and spleen, were compared. Enrichment analysis for GO and KEGG pathways indicated immune system activation in gills at severe infection, whereas in the head kidney a broad immune suppression included deactivation of cytokines and GATA3 transcription factor responsible for T helper cell differentiation. In the spleen, the cytotoxic effector proteins perforin and granzyme B were downregulated and insulin, which may function as an immunomodulatory hormone inducing systemic immune suppression, was upregulated. These findings suggest that M. bejeranoi is a highly efficient parasite that disables the defense mechanisms of its fish host hybrid tilapia.

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.…”