Integrative transcriptomic and metabolomic analyses reveal preliminary molecular mechanisms of gills response to salinity stress in Micropterus salmoides

Abstract

Salinity is a key aquatic environmental factor that affects the physiological functions of freshwater fishes through osmotic regulation. Micropterus salmoides, A euryhaline fish, shows potential for saline aquaculture; however, the molecular mechanisms underlying gill acclimation to long-term salinity stress remain poorly understood. This study investigated M. salmoides gills in salinity 0 ‰ (control), 5 ‰, 10 ‰ exposed for 24 and 48 days using histological, physiological, transcriptomic, and metabolomic approaches. Histological examination revealed that salinity stress induced curvature and deformation of gill lamellae, thinning of gill filaments at 5 ‰ salinity, while lamellar tips exhibited enlargement at 10 ‰ salinity. Furthermore, NKA activity was significantly lower in the salinity-exposed groups than in the control group at both 24 and 48 days. Antioxidant activities (T-SOD, CAT, GSH-Px and T-AOC) initially increased but subsequently decreased under salinity stress. Salinity-induced oxidative stress in the gill tissues disrupted cellular membrane lipid homeostasis, ultimately triggering apoptosis. Arachidonic acid metabolism was identified as a key pathway mediating oxidative stress responses. Integrated multi-omics analyses demonstrated that the renin-angiotensin system (RAS) plays a pivotal role in long-term salinity adaptation, with cortisol, aldosterone, and prostacyclin synthase (PGIS) contributing to osmotic regulation. Activation of carbohydrate and lipid metabolism supplied essential energy for salinity stress adaptation. In conclusion, this study provides novel insights into salinity tolerance mechanisms in euryhaline fishes and offers valuable information for developing M. salmoides saline aquaculture.