Gut microbial community plasticity as a climate shield mediating sea cucumber resilience to ocean acidification and warming

Ocean acidification (OA) and ocean warming (OW) pose escalating threats to marine ecosystems, particularly to benthic organisms, such as sea cucumbers, that play pivotal roles in nutrient cycling and sediment health. Existing research mainly addresses sea cucumbers' physiological responses, overlooking gut microbial communities and metabolites in their stress adaptation. Herein, a mesocosm was constructed and analyzed by using integrated gut microbiome and metabolomics approaches to investigate the responses of sea cucumbers <i>Apostichopus japonicus</i> to OA and OW. Results revealed that microbial community plasticity underpins holobiont adaptation, with warming restructuring gut microbiota toward thermotolerant taxa, whereas acidification enriches alkalinity-modulating Rhodobacteraceae and <i>Halioglobus</i> sp. Metabolomic profiling identified 43 amino acid derivatives with significantly increased concentrations in OA and OW groups, including upregulated N-methyl-aspartic acid and γ-glutamyl peptides that stabilize macromolecules and enhance redox homeostasis. Conversely, antioxidative metabolites (e.g., ergothioneine, L-homocystine) are suppressed, reflecting trade-offs between energy allocation and stress protection. In OW group, the antioxidant synthesis pathway is shifted to energy metabolism related to heat tolerance, whereas in OA group, energy is preferentially used for alkalinity regulation pathways rather than oxidative stress defense. Changes in microbial community structure mechanistically explain the trends in metabolite concentrations, as the proliferation of <i>Vibrio</i> spp. in the OW group drives lysine catabolism, leading to a significant increase in L-saccharopine levels. Bacteroidetes reduction in the OA group correlates with L-homocystine downregulation, suggesting that pH-driven microbial interactions are disrupted. These findings demonstrate gut microbiota reshape community structure and metabolism to mitigate synergistic climate stress, emphasizing microbiome-mediated resilience in marine ecosystems amid global climate change.