Temperature acts as a primary architect of microbial life in the deep biosphere, yet the systematic reorganization of metabolic strategies across extreme thermal gradients remains poorly understood. Using the Guaymas Basin as a natural laboratory, we analyzed 722 non-redundant metagenome-assembled genomes (MAGs) across a 4–87°C gradient to resolve the functional logic of microbial thermal adaptation. Our results reveal a sharp, temperature-driven metabolic bifurcation: cool-sediment communities (4–20°C) exhibit a scavenging-oriented generalist strategy, supported by an expansive repertoire of resource acquisition, environmental sensing, and complex organic catabolism genes. This high-cost regulatory investment is fueled by the high energy yield of aerobic respiratory potential. In contrast, hot-sediment communities (>45°C) undergo a fundamental shift toward maintenance-oriented bioenergetic specialization. This streamlined strategy is marked by the modular enrichment of F₄₂₀-dependent redox systems and an enhanced investment in genome integrity and protein quality control. Across this gradient, functional continuity in sulfur and hydrogen cycling is maintained despite profound changes in microbial community composition. Collectively, these findings demonstrate that the microbial response to thermal stress is not a gradual replacement of one microbial species by another, but a systematic reallocation of energy budgets among major microbial clades. This study provides a universal framework for understanding how temperature-driven bioenergetic constraints shape the functional architecture and biogeochemical resilience of the deep sedimentary biosphere.

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