Divergence of underlying mechanisms in response to alkalinity conditions between two crucian carp (Carassius auratus) populations

Climate change and anthropogenic activities are accelerating the global expansion of saline-alkaline water. High-alkalinity is a dominant stressor threatening aquatic organism survival and reproduction. Understanding the mechanism underlying alkalinity tolerance is essential for assessing the adaptive potential and guiding molecular breeding for saline alkaline aquaculture. Here, we investigated the divergence of physiological and molecular responses to different alkalinity conditions between freshwater (PX) and alkaline water (DL) populations of Carassius auratus , a species exhibiting high-alkalinity plasticity. The PX and DL populations showed significant alkalinity adaptive divergence: both showed high adaptability to low- and moderate-alkalinity, but the DL population showed superior tolerance to high-alkalinity. Alkalinity-responsive and population-divergent genes and metabolites were enriched in energy and ammonia metabolism-related shared pathways, including amino sugar and nucleotide sugar metabolism, lipid metabolism, nitrogen metabolism and alanine, aspartate and glutamate metabolism. In contrast to the PX population, the urea cycle and transamination were enhanced in the DL population, whereas amino sugar and nucleotide sugar metabolism, amino acid oxidation and glycolysis were suppressed under alkalinity stress. Carbamoyl-phosphate synthase upregulation and glutaminase downregulation indicated enhanced ammonia detoxification for alkalinity adaptation in the DL population. Downregulation of glutamine-fructose-6-phosphate transaminase 1 and hexokinase, coordinated with upregulation of stearoyl-CoA desaturases and alanine aminotransferase ( ALT ), revealed an active energy adjustment. ALT may serve as a crucial regulator of amino acid utilization for energy production and ammonia control. These findings provide novel insights into the mechanisms underlying alkalinity adaptation and establish a foundation for sustainable aquaculture development in saline alkaline ecosystems. • The DL population of Carassius auratu s exhibits superior high-alkalinity tolerance compared to the freshwater PX population. • Population-specific trade-offs between ammonia detoxification and energy homeostasis strategies were revealed. • ALT may serve as a crucial regulator, balancing energy production and ammonia control. • We proposed potential molecular targets for breeding alkalinity-resilient fish.