Differential Modulation of IgT and IgM upon Parasitic, Bacterial, Viral, and Dietary Challenges in a Perciform Fish

Abstract

Three different immunoglobulin (Ig) isotypes can be found in teleost fish, IgM, IgD, and the teleost-specific IgT. IgM is considered to have a systemic activity, and IgT is attributed a mucosal role, similar to mammalian IgA. In this study, the complete sequence of gilthead sea bream IgM and IgT in their membrane (m) and soluble (s) forms are described for the first time in a perciform fish. Their constitutive gene expression is analyzed in different tissues, and their regulation upon viral, bacterial, parasitic, mucosal vaccination and dietary challenges are studied. GCB IgM and IgT have the prototypical structure when compared to other fish Igs. The constitutive expression of sIgM was the highest overall in all tissues, whereas mIgT expression was highest in mucosal tissues, such as gills and intestine. IgM and IgT were differentially regulated upon infection. IgT was highly upregulated locally upon infection with the intestinal parasite Enteromyxum leei or systemically after Nodavirus infection. Long-term intestinal parasitic infections increased the serum titer of both isotypes. Mucosal vaccination against Photobacterium damselae subsp. piscicida finely regulated the Ig response inducing a systemic increase of IgM titers in serum and a local IgT response in skin mucus when animals were exposed to the pathogen by bath challenge. Interestingly, plant-based diets inhibit IgT upregulation upon intestinal parasitic challenge, which was related to a worse disease outcome. All these results corroborate the mucosal role of IgT and emphasize the importance of a finely tuned regulation of Ig isotypes upon infection, which could be of special interest in vaccination studies.

Water temperature, time of exposure and population density are key parameters in Enteromyxum leei fish‐to‐fish experimental transmission

“…Interestingly, despite the higher parasite prevalence at the posterior intestine in T1, there was a slower progression of the infection along the intestinal tract than in T2, which could be due to the higher levels of specific antibodies observed at high temperatures. Previous studies have described the important role of IgM in E. leei ‐GSB infections, with an overexpression of IgM in posterior intestine and head kidney in infected GSB (Piazzon et al, ). Another study showed that GSB that survived an infection with E. leei showed high levels of parasite‐specific IgM in serum, even several months after eliminating the parasite (Picard‐Sánchez et al, ).…”

Comprehensive overview of feed‐to‐fillet transfer of new and traditional contaminants in Atlantic salmon and gilthead sea bream fed plant‐based diets

“…However, carnivorous fish fed with little or no fish meal/fish oil diets have been shown to have a wide range of metabolic effects that, in addition to affecting growth performance, can also impact on health (Martin & Król, ; Torrecillas et al., ) or the nutritious value of seafood products as the most important source of omega‐3 in the human diet (Ballester‐Lozano, Benedito‐Palos, Mingarro, Navarro, & Pérez‐Sánchez, ; Ballester‐Lozano et al., ; Benedito‐Palos et al., ). The precise mechanisms for this disruption of fish health and welfare are not fully understood, although recent studies with extreme diet formulations pointed out in gilthead sea bream that dietary supplementation of plant‐based diets with sodium butyrate helps to prevent in long‐term feeding trials the inflammation of the intestinal epithelium, preserves the integrity of the intestinal barrier (Estensoro et al., ) and improves bacteria and parasite disease outcomes (Piazzon et al., , ). Samples from these fish within the ARRAINA project and previous Atlantic salmon and gilthead sea bream from AQUAMAX trials have been used to assess the impact of the combined and maximized replacement of marine feed sources by plant ingredients on the feed‐to‐fillet transfer of contaminants (Table shows the ingredients and chemical composition of aquafeeds).…”

Stearoyl-CoA desaturase (scd1a) is epigenetically regulated by broodstock nutrition in gilthead sea bream (Sparus aurata)

“…However, high inclusion levels of plant-ingredients are often related with a pro-inflammatory condition with a negative impact on fish health and stress resilience [7][8][9][10]. Plant-based diets can also alter the normal sex proportion ratio, enhancing the male-female reversal in the protandric gilthead sea bream as the result of less powerful functional females during the reproduction period [11].…”