Integration of metabolomic and transcriptomic analyses to characterize the influence of the gill metabolism of Nibea albiflora on the response to Cryptocaryon irritans infection

Abstract

The parasite Cryptocaryon irritans causes massive losses in the marine fish culture industry and is one of the most threatening pathogens affecting teleost species. The acute death of infected fish is primarily caused by the destruction of gill cells, resulting in osmotic imbalance and respiratory stress. C. irritans has wide host specificity; however, the yellow drum Nibea albiflora is highly resistant to this parasite. Metabolomic approaches in combination with transcriptomic analysis were used to characterize the host immune reaction and metabolic changes in yellow drum in response to C. irritans infection and to identify the key genes and compounds in the gills that have the strongest contribution to disease resistance. The yellow drum was challenged with theronts at a median death rate (2050 theronts per gram fish). The samples were collected from the gills 24 h and 72 h after the infection (hpi). The results of metabolomic analysis indicated that metabolites involved in energy metabolism were predominantly downregulated. In contrast, a compensatory increase in the expression of the genes involved in the citric acid cycle and glycolysis was detected 24 hpi. The suppression of metabolites was alleviated after feed intake recovery 72 hpi. The levels of amino acids were decreased, and the expression of aminoacyl-tRNA was increased. Additionally, elevated levels of arachidonic acid derivatives, primarily prostaglandins, were responsible for anti-inflammatory, osmotic, and hypoxia regulations. Purine metabolism was also involved in the immune response via generation of reactive oxygen species catalyzed by xanthine oxidase. A significant increase in the generation of retinoic acid, which could enhance mucosal adaptive immunity by stimulating the synthesis of antibodies and accelerating the restoration of epithelial integrity, was observed at 72 hpi. This result was consistent with high expression of the genes related to secreted immunoglobulin T 72 hpi. In conclusion, the present study comprehensively described the key compounds and genes related to C. irritans infection in yellow drum gills. Biomarkers that were significantly changed during the infection may represent future targets for nutritional intervention to enhance host immunity against C. irritans infection and to accelerate disease recovery.