Oxidative stress, inflammation, and apoptosis contribute to the pathogenesis of Amyloodinium ocellatum infection in yellowfin seabream (Acanthopagrus latus)

Abstract

Amyloodinium ocellatum is a pathogenic parasitic dinoflagellate that infects most marine fish, including the Acanthopagrus latus. This study combined transcriptomics and metabolomics analyses to investigate the pathogenesis of A. ocellatum infection in A. latus. The results indicated that A. ocellatum infection significantly up-regulated 1,556 genes and 326 metabolites while down-regulating 1,668 genes and 399 metabolites in the gills of A. latus. The Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses revealed that numerous differentially expressed genes (DEGs) and differential metabolites (DMs) were enriched in pathways associated with oxidative stress, inflammation, and apoptosis, suggesting that these factors may be key drivers of disease pathogenesis and mortality in infected fish. The effects of A. ocellatum infection on reactive oxygen species (ROS) levels, apoptosis, antioxidant capacity, and gene expression in the gills of A. latus were also investigated, alongside hematological and histopathological analyses of the internal organs. The results revealed that A. ocellatum infection induced overproduction of ROS, triggering apoptosis, altered oxidase and antioxidant enzyme activities, and increased mRNA expression of inflammation-related (COX-2, IL-1β, IL-8) and apoptosis-related genes (CatB, CASP3) in the gills of A. latus. Moreover, cholesterol (CHO) concentrations and aspartate transaminase (AST) activity in the serum, as well as the number and density of melanomacrophage centers (MMCs) in the spleen, were significantly higher (P < 0.05) in the infected fish. In conclusion, this study reports that A. ocellatum infection causing oxidative stress, inflammation, and apoptosis in the gills of A. latus, which contribute to fish mortality.