Rapid ecosystem collapse and biofilter formation following seabed methane leakage

Globally, vast amounts of methane are trapped within subseafloor gas hydrates1. Recent evidence suggests that climate- and human-induced perturbations can destabilize gas hydrates and trigger methane release2-5, yet the response of deep-sea ecosystems to these changes remains poorly understood. Here we show multi-year in situ monitoring of seabed ecosystem following methane leakage induced by hydrate exploration activities. Within just two years, benthic microbial and eukaryotic diversity in the affected areas declined significantly, while microbial and macrofaunal abundance increased. Integrated geochemical and omics analyses reveal the rapid successional shift of seabed ecosystem to a novel chemosynthetic system. Aerobic methanotrophs (Methyloprofundus) co-established with unexpectedly fast growing anaerobic methanotrophic archaea (ANME-3), accompanied by a rapid recruitment of opportunistic polychaetes that bioirrigated the seabed to >50 cm depths. The active animal-microbe interactions sustained exceptionally high rates of methane oxidation that utilized diverse electron acceptors. We demonstrate that methane hydrate destabilization can trigger rapid collapse of native seabed ecosystem while driving the formation of an effective "methane biofilter" consuming this potent greenhouse gas much faster than previously estimated. Understanding seabed ecosystem response and feedback is critical for predicting benthic methane cycling under ongoing global change and for developing sustainable strategies for methane hydrate resource management.