Rapid de novo assembly of animal-microbe biofilter to mitigate seabed methane leakage

ABSTRACT Anthropogenic and climatic perturbations threaten to destabilize gas hydrates and release methane from its vast subseafloor reservoir. Yet the deep-sea ecosystem responses remain poorly understood. Our multi-year, in situ monitoring of a human-induced methane seep unveiled an exceptionally fast, de novo establishment of a methane-consuming ecosystem within 1–2 years, followed by a rapid succession toward natural mature seeps. Integrated biogeochemical and molecular analyses revealed an unexpectedly parallel proliferation of aerobic methanotrophs (Methyloprofundus), anaerobic methanotrophs (ANME-2e, ANME-3), and opportunistic fauna bioturbating the seabed to >50 cm depths. Within this intensively mixed zone, active animal-microbe interactions sustained rapid methane removal (30–60 mmol/m2/day) through intricate carbon, nitrogen, and sulfur redox coupling. Our work demonstrates that abrupt methane leakage can form an effective animal-microbe ‘methane biofilter’ far quicker than previously estimated, producing new insights into benthic natural mitigation capacity and limit that are critical for risk assessments and climate projections under increasing seabed methane efflux.