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

Abstract 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 studies have mostly focused on the physiological responses of sea cucumbers, yet overlooked the critical roles of both gut microbial communities and metabolites in the host's responses under environmental stress. Herein, a mesocosm experiment was constructed and analyzed by using integrated gut microbiome and metabolomics approaches to investigate the responses of sea cucumbers Apostichopus japonicus 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 Halioglobus sp.. Metabolomic profiling identified 43 amino acid derivatives that exhibit significantly increased concentrations in the OA and OW groups. These derivatives include upregulated N-methyl-aspartic acid and γ-glutamyl peptides, which stabilize macromolecules and enhance redox homeostasis. Conversely, antioxidative metabolites, such as ergothioneine and 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 Vibrio spp. in the OW group drives lysine catabolism, leading to a significant increase in L-saccharopine levels. The reduction of Bacteroidetes in the OA group is correlated with the downregulation of L-homocystine, suggesting that pH-driven microbial interactions are disrupted. These findings demonstrate that gut microbiota reconfigure community structure and metabolic landscapes to buffer hosts against climate stress synergies, highlighting the importance of microbiome-mediated resilience in marine ecosystems under global climate change.