The abyssal ocean harbours active microbial communities despite high hydrostatic pressure (HHP), hypoxia, and chronic energy limitation—conditions that together constitute the deep-sea energy limitation paradox. How these communities maintain viability while sustaining the metabolic costs of pressure adaptation remains unresolved. Here, integrating global marine metagenomics across oceanic depth and oxygen gradients, we reveal a ubiquitous enrichment of branched-chain amino acid (BCAA) catabolic pathways in energy-limited marine environments. To elucidate the physiological basis of this trait, we performed enrichment incubations of northwestern Pacific abyssal sediments (5,950.8 m) at distinct pressures treatments (0.1 MPa vs. 40 MPa), revealing strong pressure dependent selection for BCAA degradation, particularly under hypoxia. Transcriptomic profiling of the deep-sea isolate Pseudomonas sp. mechanistically confirms this reliance, showing coordinated HHP-induced up-regulation of BCAA catabolism and transport concomitant with suppression of glycolysis. Maximum-likelihood ancestral state reconstruction demonstrates that high-affinity BCAA transport capacity was acquired via horizontal gene transfer into diverse ancestral deep-sea clades, marking a pivotal evolutionary adaptation to the deep-sea energy limitation paradox. The parallel induction of membrane-remodelling and solute-transport genes establishes a dual function for BCAAs: serving simultaneously as primary anaerobic energy substrates and as compatible solutes providing biophysical stability under compressive force. Collectively, our results demonstrate that the evolutionary acquisition of BCAA transport represents a fundamental microbial adaptation, providing the energetic and biophysical stability necessary to thrive in Earth's extreme deep-ocean biosphere.

 

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