Transcriptome and serum metabolites analysis revealed tissue-specific response pathways to acute salinity stress in grass carp

Abstract

Salinity is a key environmental factor affecting the survival of teleost fish. Understanding the response of fish to salinity fluctuations, especially the expression patterns and regulatory mechanisms in different tissues, is crucial for the breeding of salt-tolerant fish strains. This study evaluated the tolerance mechanisms of grass carp (Ctenopharyngodon idella) under acute salinity stress, with a focus on the gills, kidneys, and skin, using histological evaluation, physiological and biochemical assessments, and transcriptomic profiling. To achieve this objective, both serum and tissue samples were collected for comprehensive analysis. The results indicated salinity stress induced pathological changes and oxidative damage in the tissues. Transcriptomic analysis revealed that after 24 h of exposure to 9 ppt salinity stress, 306, 1241, and 259 differentially expressed genes (DEGs) were identified in the gills, kidneys, and skin, respectively, the overlapping genes among which were significantly associated with secondary active transmembrane transporter activity. Furthermore, enrichment analysis revealed that while the gills primarily activated mechanisms related to lipid metabolism, such as glycosphingolipid biosynthesis and steroid hormone biosynthesis, the kidneys, in contrast, mainly activated pathways associated with cell fate regulation, including the Notch and ErbB signaling pathways, to cope with salinity stress. Conversely, the skin mostly initiated intracellular degradation pathways under salinity stress, such as the proteasome and autophagy pathways. Moreover, the key DEGs identified in the tissues were strongly correlated with the differentially expressed metabolites (DEMs) in the serum, suggesting that the salt tolerance of fish in saline environments is the result of the coordinated function of multiple organs. In conclusion, the findings of this study provide insights into the tissue-specific responses of grass carp to salinity stress, further offering a theoretical basis for breeding salt-tolerant grass carp strains.