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Published February 12, 2016 | Supplemental Material
Journal Article Open

Artificial electron acceptors decouple archaeal methane oxidation from sulfate reduction

Abstract

The oxidation of methane with sulfate is an important microbial metabolism in the global carbon cycle. In marine methane seeps, this process is mediated by consortia of anaerobic methanotrophic archaea (ANME) that live in syntrophy with sulfate-reducing bacteria (SRB). The underlying interdependencies within this uncultured symbiotic partnership are poorly understood. We used a combination of rate measurements and single-cell stable isotope probing to demonstrate that ANME in deep-sea sediments can be catabolically and anabolically decoupled from their syntrophic SRB partners using soluble artificial oxidants. The ANME still sustain high rates of methane oxidation in the absence of sulfate as the terminal oxidant, lending support to the hypothesis that interspecies extracellular electron transfer is the syntrophic mechanism for the anaerobic oxidation of methane.

Additional Information

© 2016 American Association for the Advancement of Science. Received 26 October 2015; accepted 20 January 2016. We thank Y. Guan for assistance with the nanoSIMS, the Beckman Resource Center (BRCem) for sectioning, M. Aoki for FISH analysis of ANME-2a and ANME-2c consortia, and S. Goffredi and C. Skennerton for editorial comments. We are grateful to P. Brewer from the Monterey Bay Aquarium Research Institute for providing the opportunity to participate in the 2013 research expedition and A. Pasulka and K. Dawson for their contributions in shipboard sample processing. This work was supported by the U.S. Department of Energy Biological and Environmental Research program (grants DE-SC0010574 and DE-SC0004940) and funding by the Gordon and Betty Moore Foundation through grants GBMF3306 and GBMF3780 (to V.J.O.). S.S. was supported in part by the Swiss National Science Foundation (grant no. PBEZP2_142903). All data are available in the supplementary materials. Archaeal 16S rRNA, mcrA genes, and bacterial 16S rRNA genes were deposited with the National Center for Biotechnology Information under accession numbers KU324182 to KU324260, KU324346 to KU324428, and KU324261 to KU324345, respectively. S.S., H.Y., and V.J.O. devised the study, and S.S., H.Y., G.L.C., and S.M. conducted the experiments and analyses. S.S. and V.J.O. wrote the manuscript, with contributions from all authors to data analysis, figure generation, and the final manuscript.

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