Promoter methylation as a potential cause for the decrease in pyruvate metabolism during environmentally induced aestivation in Apostichopus japonicus

Apostichopus japonicus is an important aquaculture species with significant economic value. As water temperatures increase during the summer, A. japonicus enters aestivation to resist adverse environments and maintain survival. The most significant feature of aestivation in sea cucumbers is metabolic depression, but the molecular mechanisms involved in this process are not fully explained. In this study, we analyzed the methylation status and gene expression of intestinal tissues from A. japonicus during aestivation, to reveal the mechanism of metabolic depression involved during aestivation from the perspective of epigenetic modifications. Of the 2886 hypermethylated genes and 1534 hypomethylated genes obtained, methylation and transcriptome correlation analysis identified 207 methylation-driven low-expression candidate genes and 71 methylation-driven highly expressed candidate genes. Analysis of the methylation location showed that 5% of differential methylation occurred in the promoter region; those genes that were differentially methylated in the promoter region were also significantly enriched in the pyruvate metabolic pathway. Metabolite content analysis of the glycolytic pathway and the tricarboxylic acid cycle pathway, key sources and consumption pathways of pyruvate, respectively, showed that the content of these metabolites was significantly reduced, suggesting pyruvate metabolic depression of A. japonicus during aestivation. In conclusion, these results reveal that promoter methylation is likely a potential cause of pyruvate metabolic depression during aestivation in A. japonicus. They also provide new insights into the epigenetic regulation mechanism of hypometabolism during aestivation.