Immunoprotective role of fish mucus against the ectoparasitic flatworm Sparicotyle chrysophrii

The gill ectoparasite, Sparicotyle chrysophrii, has a significant impact on gilthead seabream farming in the Mediterranean. Yet, it remains unclear whether gilthead seabream develops immunological memory and protection following exposure to the parasite, which causes severe anaemia by feeding on the host's blood. This study compared recovered gilthead seabream (RE), which had overcome sparicotylosis, and naïve fish (NAI), never exposureed to the parasite. Both groups were exposed to S. chrysophrii eggs, and parasitic burdens, biometric and haematological parameters were monitored over 62 days post-exposure (dpe). Total and specific IgM and IgT titers were measured in plasma and gill mucus by ELISA, binding specificity of specific immunoglobulins were determined by immunohistochemistry, and immunoglobulin-expressing cells were quantified in spleens and gills of RE and NAI fish. Infection outcome, haematological parameters and fish fitness were worse in NAI than in RE fish. Results showed a strong mucosal immune response in RE gills, with high local secretion of parasite-specific immunoglobulins, particularly IgT, which were absent in NAI and undetectable in plasma of all recipient fish. Five months after the initial exposure, RE gill mucus still had significantly higher specific IgM and IgT titers than NAI. However, after the secondary exposure, these titres gradually decreased in RE, eventually becoming significantly lower than in NAI by the end of the trial. Immunohistochemistry confirmed the binding specificity of anti-S. chrysophrii IgT in RE gill mucus and IgM in plasma. Additionally, RE showed a higher number of IgT-expressing cells in the gills and IgM-expressing cells in the spleen.