Host-intestinal microbiota interactions in Edwardsiella piscicida-induced lethal enteritis in big-belly seahorses: novel insights into the role of Carbohydrate-Active enzymes and host transcriptional responses.

Edwardsiella piscicida-induced lethal enteritis is a major threat to the sustainable development of seahorse aquaculture. The roles of Carbohydrate-Active enzymes (CAZymes) in interactions between the pathogen and the host are poorly understood. In this study, we found that 22 key CAZymes encoded by E. piscicida might involve in the coordination of five key stages of infection. Specifically, during the motility, adherence, and invasion stages, 10 CAZymes, including CE4, PL8, and CBM48, may significantly increase the activities of Lipid metabolism-associated pathways of the intestinal microbiota (P < 0.01), facilitating pathogen invasion of the host intestinal epithelium. During the replication stage, 11 CAZymes, including GH20, GT4, and GH3, may significantly increase activities of pathways associated with Carbohydrate metabolism (P < 0.01) to promote replication and proliferation of the pathogen. And for avoiding host defenses, GH2 and GH1 may enhance activities of both Carbohydrate and Amino acid metabolic pathways (P < 0.01), facilitating infection and immune evasion. Conjoint analysis showed that E. piscicida might mainly rely on Carbohydrate metabolism for infection, while the host might activate Amino acid metabolic pathways for self-defense. In addition, expressions of 10 key genes, Aldh9a1b, Aoc1, Tpi1b, PCK1, Ldha, Me1, Gla, Cel.2, Ugdh, and Mao, were significantly altered (P < 0.01) and may be used for characterizing host responses to E. piscicida infection. Activities of both Glycolysis/Gluconeogenesis and Tryptophan metabolism were found oppositely changed (P < 0.01) between pathogen and host, respectively, representing the primary focuses of the competition. Overall, this study provides new insights into E. piscicida-mediated intestinal enteritis in fish for the first time from the perspective of CAZymes, as well as a theoretical reference for the prevention and control of these diseases in the aquaculture of seahorses and other fish.