Aestivation alters gut bacterial community structure and host metabolic profiles in Apostichopus japonicus

Aestivation, a hypometabolic adaptive strategy, enables organisms to reduce energy consumption and enhance survival under high-temperature stress. However, the role of gut bacterial networks and host-bacteria co-metabolism in aestivation remains unclear. In this study, we investigated the changes in gut bacterial networks and host metabolism of aestivating A. japonicus . Significant differences were found in the gut bacterial communities between aestivating and non-aestivating sea cucumbers. The relative abundance of Proteobacteria significantly decreased from 86.59% in non-aestivating individuals to 48.71% in aestivating individuals, whereas the relative abundances of Actinobacteria, Bacteroidota, and Verrucomicrobiota significantly increased from 2.59%, 2.03%, and 1.13–5.93%, 8.06%, and 19.65%, respectively. Co-occurrence network analysis suggested a trend toward reduced network size and connectivity during aestivation, accompanied by increased modularity, although these patterns should be interpreted cautiously given the limited sample size. Further analysis showed that Proteobacteria, Bacteroidota, and Firmicutes and Enterococcus and Dubosiella might be important keystone taxa in the gut bacterial network during aestivation. Untargeted metabolomic analysis identified 155 significantly upregulated metabolites and 77 significantly downregulated metabolites in aestivating A. japonicus compared with nonaestivating individuals. These differential metabolites were primarily enriched in two distinct metabolic pathways, namely unsaturated fatty acid metabolism and amino acid metabolism. Notably, serine, oleamide, and glutamine were significantly upregulated, while isovaleric acid, arachidonic acid, and acetylcholine were significantly downregulated. Moreover, the keystone taxa, including Enterococcus and Dubosiella , were significantly correlated with the altered metabolites, such as serine, oleamide, and glutamine. These findings indicate possible links among gut bacterial community shifts, metabolic changes, and aestivation in A. japonicus. This work may provide new insights into the role of gut bacterial networks and host metabolism in A. japonicus aestivation.