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ISME J. 2018 Jan;12(1):31-47. doi: 10.1038/ismej.2017.140. Epub 2017 Sep 8.

Ecological and genomic profiling of anaerobic methane-oxidizing archaea in a deep granitic environment.

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Department of Earth and Planetary Science, Graduate School of Science, The University of Tokyo, Tokyo, Japan.
Department of Plant and Microbial Biology, University of California, Berkeley, CA, USA.
Geological Survey of Japan, National Institute of Advanced Industrial Science and Technology, Tsukuba, Ibaraki, Japan.
Graduate School of Environmental Engineering, The University of Kitakyushu, Kitakyushu, Fukuoka, Japan.
Ore Genesis Research Unit, Project Team for Development of New-generation Research Protocol for Submarine Resources, JAMSTEC (Japan Agency for Marine-Earth Science and Technology), Yokosuka City, Kanagawa, Japan.
Japan Atomic Energy Agency, Naka-gun, Ibaraki, Japan.
Graduate School of Environmental Studies, Nagoya University, Furo-cho, Chikusa-ku, Nagoya, Aichi, Japan.
National Institute of Technology, Ibaraki College, Hitachinaka-shi, Ibaraki, Japan.
Earth Sciences Division, Lawrence Berkeley National Laboratory, Berkeley, CA, USA.


Recent single-gene-based surveys of deep continental aquifers demonstrated the widespread occurrence of archaea related to Candidatus Methanoperedens nitroreducens (ANME-2d) known to mediate anaerobic oxidation of methane (AOM). However, it is unclear whether ANME-2d mediates AOM in the deep continental biosphere. In this study, we found the dominance of ANME-2d in groundwater enriched in sulfate and methane from a 300-m deep underground borehole in granitic rock. A near-complete genome of one representative species of the ANME-2d obtained from the underground borehole has most of functional genes required for AOM and assimilatory sulfate reduction. The genome of the subsurface ANME-2d is different from those of other members of ANME-2d by lacking functional genes encoding nitrate and nitrite reductases and multiheme cytochromes. In addition, the subsurface ANME-2d genome contains a membrane-bound NiFe hydrogenase gene putatively involved in respiratory H2 oxidation, which is different from those of other methanotrophic archaea. Short-term incubation of microbial cells collected from the granitic groundwater with 13C-labeled methane also demonstrates that AOM is linked to microbial sulfate reduction. Given the prominence of granitic continental crust and sulfate and methane in terrestrial subsurface fluids, we conclude that AOM may be widespread in the deep continental biosphere.

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