Metal-Driven Anaerobic Oxidation of Methane as an Important Methane Sink in Methanic Cold Seep Sediments

Anaerobic oxidation of methane (AOM) coupled with reduction of metal oxides is supposed to be a globally important bioprocess in marine sediments. However, the responsible microorganisms and their contributions to methane budget are not clear in deep sea cold seep sediments. Here, we combined geochemistry, muti-omics, and numerical modeling to study metal-dependent AOM in methanic cold seep sediments in the northern continental slope of the South China Sea. Geochemical data based on methane concentrations, carbon stable isotope, solid-phase sediment analysis, and pore water measurements indicate the occurrence of anaerobic methane oxidation coupled to metal oxides reduction in the methanic zone. The 16S rRNA gene and transcript amplicons, along with metagenomic and metatranscriptomic data suggest that diverse anaerobic methanotrophic archaea (ANME) groups actively mediated methane oxidation in the methanic zone either independently or in syntrophy with, e.g., ETH-SRB1, as potential metal reducers. Modeling results suggest that the estimated rates of methane consumption via Fe-AOM and Mn-AOM were both 0.3 mu mol cm(-2) year(-1), which account for similar to 3% of total CH4 removal in sediments. Overall, our results highlight metal-driven anaerobic oxidation of methane as an important methane sink in methanic cold seep sediments. IMPORTANCE Anaerobic oxidation of methane (AOM) coupled with reduction of metal oxides is supposed to be a globally important bioprocess in marine sediments. However, the responsible microorganisms and their contributions to methane budget are not clear in deep sea cold seep sediments. Our findings provide a comprehensive view of metal-dependent AOM in the methanic cold seep sediments and uncovered the potential mechanisms for involved microorganisms. High amounts of buried reactive Fe(III)/Mn(IV) minerals could be an important available electron acceptors for AOM. It is estimated that metal-AOM at least contributes 3% of total methane consumption from methanic sediments to the seep. Therefore, this research paper advances our understanding of the role of metal reduction to the global carbon cycle, especially the methane sink.