Integrated transcriptome and metabolome analysis reveals new insights into acclimation of sea cucumber Stichopus monotuberculatus to hypo-osmotic stress

Artificial breeding of the commercially important sea cucumber Stichopus monotuberculatus is constrained by the high sensitivity of juveniles to environmental stressors, particularly abrupt changes in salinity. However, the molecular and physiological mechanisms underlying salinity acclimation remain unclear. In this study, we integrated physiological, transcriptomic and metabolomic analyses to elucidate regulatory mechanisms of S. monotuberculatus in hypo-osmotic conditions (18‰ and 24‰) and its subsequent recovery to 30‰. The results showed that the rate of oxygen consumption and Na + /K + -ATPase activity significantly decreased under hypo-osmotic stress, indicating a state of metabolic depression in sea cucumbers. Transcriptomic and metabolomic analyses revealed that osmoregulation was primarily regulated through the catabolism of free amino acids and inorganic ion transporters under salinity fluctuation. Meanwhile, the lipid metabolism pathway was significantly enhanced, including phosphocholine biosynthesis and arachidonic acid metabolism, which suggested their potential roles in maintaining membrane integrity and immunomodulation. Furthermore, genes involved in peroxisomal fatty acid β-oxidation were significantly upregulated to compensate for the suppressed mitochondrial TCA cycle and meet energy requirements under hypo-osmotic stress. In conclusion, during salinity reduction, S. monotuberculatus primarily osmoregulates through the catabolism of free amino acids, and then switches to inorganic ion transport upon salinity recovery. Meanwhile, it adjusts its lipid and energy metabolism by activating pathways for membrane repair, immune response, and alternative energy production via fatty acid β-oxidation to maintain cellular homeostasis. These findings provide new insights into the potential osmoregulatory mechanisms in S. monotuberculatus , and deepen our understanding of sea cucumber survival strategies in dynamic environments.