Simulated cold spell: Changes of lipid metabolism on silver pomfret during cooling and rewarming

Abstract

In recent decades, frequent extreme cold spells have led to fluctuations in water temperature. As poikilotherm, fish adapt to the environmental temperature through a series of physiological and metabolic regulation. Silver pomfret (Pampus argenteus) is an economical marine fish, a potential candidate for aquaculture. To investigate the impact of cold stress and subsequent rewarming on the energy metabolism of silver pomfret, we simulated an extreme cold spell by gradually lowering water temperature from 18 °C to 6 °C, followed by a gradual rise to 12 °C. The findings revealed notable trends: as the water temperature dropped to 12 °C, there was a significant increase in fatty acid content. However, upon reaching 6 °C, the condition factor (CF) decreased, accompanied by a reduction in liver mass. During the rewarming phase, severe tissue damage was observed in both muscle and liver tissues, alongside elevated AST and ALT activity. Besides, silver pomfret consumed stored fatty acids, CF, hepatosomatic index and n-3/n-6 fatty acid ratio were higher than other groups once the water temperature returned to 12 °C. Further transcriptome sequencing of the liver revealed significant enrichment in numerous metabolism-related pathways through KEGG and GO analyses. Ten differentially expressed genes (DEGs), encoding pivotal enzymes in lipid metabolism, were identified from pathways such as the PPAR signaling pathway and fatty acid degradation. Based on these results, it was hypothesized that silver pomfret shields against injury by modulating fatty acid composition. This hypothesis found validation in P. argenteus liver cells, where acsl1, cpt1 and cpt2 were identified to facilitate lipid activation and transportation. Knocking down acsl1 impacted the utilization of lipid droplets, further affirming this mechanism. This study sheds light on the adaptive strategies of economically significant fish species in confronting extreme cold spells, providing valuable insights for future reference.