Metabolic responses to starvation in the soft-shelled turtle (Pelodiscus sinensis) revealed by integrated metabolome and transcriptome analysis

Abstract

Animals frequently suffer from starvation throughout their life cycle; however, the mobilization and utilization of energy sources can differ. To clarify the fundamental mechanisms underlying energy mobilization and metabolic adjustment in response to food deprivation in the soft-shelled turtle (Pelodiscus sinensis), eighty turtles (initial body weight, 51.81 ± 0.29 g) were subjected to starvation periods of 1 d, 4 d, 8 d, 16 d, and 32 d (referred to as S1, S4, S8, S16, and S32). The results showed that the greatest absolute loss in body composition occurred in moisture, followed by protein and lipid, respectively. Hepatic glycogen contents significantly decreased after 4 days of starvation and then remained stable. Notably, plasma glucose, cholesterol, and free fatty acid contents exhibited significant decreases from S8, while plasma triacylglycerol levels dramatically declined from S4. Gluconeogenesis-related genes (pepck, g6pase) were upregulated in the starving turtles to maintain glucose homeostasis. Comparative analyses between S32 and S1 groups identified a total of 6051 differential genes and 150 differential metabolites, highlighting three overlapping metabolic pathways: glycerophospholipid metabolism, alanine, aspartate, and glutamate metabolism, and taurine and hypotaurine metabolism. Integrative analyses further revealed increased levels of specific metabolites, including phosphatidylcholine, phosphatidylethanolamine, glycerophosphocholine, L-2-aminoethyl seryl phosphate, l-serine-phosphatidylethanolamine, adenyiosuccinate, 5-phosphoribosylamine, and taurine. These metabolites are vital for amino acid-driven gluconeogenesis, cell membrane stability, and mitigating cellular damage resulting from food deprivation. In conclusion, glucose homeostasis was maintained by enhancing gluconeogenesis in P. sinensis during extended periods of starvation, and the activation of lipid and amino acid metabolism represents an adaptive metabolic strategy employed by P. sinensis to cope with starvation conditions.