Dual-Axis Life-History Framework Explains Metabolite Exchange and Functional Differentiation in Nodule Microbiomes

Background Deep-sea polymetallic nodule fields are among the most oligotrophic and metal-stressed ecosystems on Earth, where microbial communities play critical roles in driving elemental cycling and maintaining ecosystem stability. However, how environmental stress and resource limitation shape microbial life-history strategies and metabolic interactions in these systems remains poorly understood. Results We investigated the community structure, metabolic potential, and life-history strategies of microbial assemblages inhabiting polymetallic nodules and surrounding sediments by reconstructing 314 high-quality, non-redundant metagenome-assembled genomes (MAGs). Compared to sediment communities, nodule-associated microbes exhibited higher taxonomic novelty and niche specificity, with enrichment of archaeal lineages such as Nitrosopumilaceae. Both habitats harbored broad-spectrum metal resistance genes, predominantly maintained through vertical inheritance, while nodule-inhabiting microbes showed significant enrichment of resistance genes targeting arsenic, chromium, and lead. Functional analyses revealed a spatial division of labor characterized by a “specialization–buffering” relationship, with differentiated contributions to carbon, nitrogen, and sulfur cycling. Metabolic exchange network analysis indicated that sediment microbes engaged in more active exchange of energetic metabolites, including acyl-CoA and amino acids. Taxa with multifunctional life-history strategies (SY, AY, and AS) enhanced energy flow and network stability through intensified organic carbon and amino acid transfer, reflecting functional redundancy and ecological resilience. In contrast, nodule-associated communities, dominated by AS and Y strategies, primarily exchanged small organic acids and inorganic ions, consistent with adaptations toward resource efficiency and environmental persistence. Conclusions These results demonstrate that metabolic strategic differentiation in deep-sea nodule ecosystems reflects a dynamic trade-off between resource availability and environmental stress. Our dual-axis life-history framework provides a new ecological perspective on how functional stability is maintained in deep-sea extreme environments.