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

Xi Xiao; Min Luo; Chuwen Zhang; Tingting Zhang; Xiuran Yin; Xuemin Wu; Jing Zhao; Jun Tao; Zongheng Chen; Qianyong Liang; Xiyang Dong

doi:10.1128/spectrum.05337-22

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

Microbiol Spectr. 2023 Mar 28;11(2):e0533722. doi: 10.1128/spectrum.05337-22. Online ahead of print.

Authors

Xi Xiao^{1

2

3}, Min Luo⁴, Chuwen Zhang⁵, Tingting Zhang^{1

2

3}, Xiuran Yin^{6

7}, Xuemin Wu^{1

2

3}, Jing Zhao^{1

2

3}, Jun Tao¹, Zongheng Chen², Qianyong Liang^{1

2

3}, Xiyang Dong⁵

Affiliations

¹ National Engineering Research Center of Gas Hydrate Exploration and Development, Guangzhou, China.
² Key Laboratory of Marine Mineral Resources, Ministry of Natural Resources, Guangzhou Marine Geological Survey, China Geological Survey, Guangzhou, China.
³ Southern Marine Science and Engineering Guangdong Laboratory (Guangzhou), Guangzhou, China.
⁴ Shanghai Engineering Research Center of Hadal Science and Technology, College of Marine Sciences, Shanghai Ocean University, Shanghai, China.
⁵ Key Laboratory of Marine Genetic Resources, Third Institute of Oceanography, Ministry of Natural Resources, Xiamen, China.
⁶ Faculty of Biology/Chemistry, University of Bremen, Bremen, Germany.
⁷ MARUM, Center for Marine Environmental Sciences, University of Bremen, Bremen, Germany.

Abstract

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 μmol cm^-2 year^-1, which account for ~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.

Keywords: anaerobic oxidation of methane; cold seep; dissimilatory metal reduction; methane budget.