Multi-omics and biochemical analyses provide insights into hepatic glucolipid metabolism in red tilapia ( Oreochromis spp.) under salinity stress

Freshwater resources are in short supply, so the use of brackish water and seawater for aquaculture is an important strategy to address this issue. Red tilapia (Oreochromis spp.) is a valuable model organism for researching how freshwater fish respond to salinity stress as its vast salinity tolerance properties. Nevertheless, few studies have explored the responses of red tilapia, especially at the molecular level, to salinity stress. To explore the molecular mechanisms underlying the responses to prolonged salinity stress, red tilapia (average body weight: 4.62 +/- 0.10 g) were grown under a range of salinities [0 %o (control, S0), 4 %o (S4), 8 %o (S8), 12 %o (S12), 16 %o (S16), and 20 %o (S20)] for 90 days, and liver samples were taken for histological, physiological, transcriptomic, and metabolomic analyses. The fish grown under salinity levels of 8 %o-12 %o showed the best health and growth performance, as determined by analyses of growth, liver damage, and hepatocyte apoptosis. As the salinity level increased, the antioxidant capacity and energy metabolism decreased and then increased. The S8 group had considerably lower SOD and CAT activities than the other 5 groups (P < 0.05), and the S12 group had lowest TAOC and GSH-PX activities. The NKA and CMA activities were lower both in the S8 and S12 groups. Transcriptome analyses of liver tissues from fish grown under three different salinity levels (0 %o, 12 %o, and 20 %o) revealed a total of 10,360 DEGs, including 5531 up-regulated and 4829 down-regulated genes. Chronic salinity stress caused alterations in the transcript levels of important genes such as srd5a1, tecr, sc5d and elovl6, and affected the steroid hormone biosynthesis pathway, the fatty acid elongation pathway, the arachidonic acid metabolism pathway, and the ascorbate and aldarate metabolism pathway, among others. Metabolomic analyses revealed metabolites showing significant changes in abundance under salinity stress, including glucuronic acid, gluconic acid, lecithin, sphingomyelin, UDP-galactose, and hypercitric acid. Combined transcriptomic and metabolomic analyses indicated that the arachidonic acid metabolic pathway might contribute to lipid accumulation in the liver of red tilapia under salinity stress, and that low transcript levels of ptgr, hpdg and ptges genes, which encode negative regulators, led to the accumulation of 15-keto-PGF2 alpha and 13.14-dihydro-15keto-PGE2. Our findings provide fresh information about the molecular mechanisms involved in red tilapia response to salinity stress, as well as theoretical recommendations for selection and breeding of new salt-tolerant strains.