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Archaea catalyze iron-dependent anaerobic oxidation of methane

Ettwig, Katharina F. and Zhu, Baoli and Speth, Daan and Keltjens, Jan T. and Jetten, Mike S. M. and Kartal, Boran (2016) Archaea catalyze iron-dependent anaerobic oxidation of methane. Proceedings of the National Academy of Sciences of the United States of America, 113 (45). pp. 12792-12796. ISSN 0027-8424. PMCID PMC5111651. http://resolver.caltech.edu/CaltechAUTHORS:20161215-103147761

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Abstract

Anaerobic oxidation of methane (AOM) is crucial for controlling the emission of this potent greenhouse gas to the atmosphere. Nitrite-, nitrate-, and sulfate-dependent methane oxidation is well-documented, but AOM coupled to the reduction of oxidized metals has so far been demonstrated only in environmental samples. Here, using a freshwater enrichment culture, we show that archaea of the order Methanosarcinales, related to “Candidatus Methanoperedens nitroreducens,” couple the reduction of environmentally relevant forms of Fe^(3+) and Mn^(4+) to the oxidation of methane. We obtained an enrichment culture of these archaea under anaerobic, nitrate-reducing conditions with a continuous supply of methane. Via batch incubations using [^(13)C]methane, we demonstrated that soluble ferric iron (Fe^(3+), as Fe-citrate) and nanoparticulate forms of Fe^(3+) and Mn^(4+) supported methane-oxidizing activity. CO_2 and ferrous iron (Fe^(2+)) were produced in stoichiometric amounts. Our study connects the previous finding of iron-dependent AOM to microorganisms detected in numerous habitats worldwide. Consequently, it enables a better understanding of the interaction between the biogeochemical cycles of iron and methane.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://dx.doi.org/10.1073/pnas.1609534113DOIArticle
http://www.pnas.org/content/113/45/12792PublisherArticle
http://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1609534113/-/DCSupplementalPublisherSupporting Information
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5111651/PubMed CentralArticle
Additional Information:© 2016 National Academy of Sciences. Edited by Donald E. Canfield, Institute of Biology and Nordic Center for Earth Evolution, University of Southern Denmark, Odense M, Denmark, and approved September 16, 2016 (received for review June 13, 2016). Published online before print October 24, 2016. We thank Francisca A. Luesken for starting and initially maintaining the AAA enrichment culture. K.F.E. was supported by a VENI grant from The Netherlands Organization for Scientific Research (863.13.007), B.Z. by the joint program of the Chinese Academy of Science/Royal Dutch Academy of Science (09PhD02), D.S. by the BE-Basic Foundation (fp07.002), M.S.M.J. by the European Research Council (ERC 339880) and the Spinoza Prize, and B.K. by a VENI grant from The Netherlands Organization for Scientific Research (863.11.003) and the European Research Council (ERC 640422). Author contributions: K.F.E., B.Z., M.S.M.J., and B.K. designed research; B.Z. and D.S. performed research; D.S. carried out sequencing and genome assembly; K.F.E., B.Z., J.T.K., M.S.M.J., and B.K. analyzed data; and K.F.E. and B.K. wrote the paper. The authors declare no conflict of interest. This article is a PNAS Direct Submission. Data deposition: The sequence reported in this paper has been deposited in the DDBJ/EMBL/GenBank database (metagenome accession no. LKCM01000000). This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1609534113/-/DCSupplemental.
Funders:
Funding AgencyGrant Number
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)863.13.007
Chinese Academy of SciencesUNSPECIFIED
Royal Dutch Academy of Science09PhD02
BE-Basic Foundationfp07.002
European Research Council (ERC)339880
Spinoza PrizeUNSPECIFIED
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)863.11.003
European Research Council (ERC)640422
Subject Keywords:anaerobic oxidation of methane; archaea; iron reduction; manganese reduction; multiheme proteins
PubMed Central ID:PMC5111651
Record Number:CaltechAUTHORS:20161215-103147761
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20161215-103147761
Official Citation:Katharina F. Ettwig, Baoli Zhu, Daan Speth, Jan T. Keltjens, Mike S. M. Jetten, and Boran Kartal Archaea catalyze iron-dependent anaerobic oxidation of methane PNAS 2016 113 (45) 12792-12796; published ahead of print October 24, 2016, doi:10.1073/pnas.1609534113
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:72844
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:15 Dec 2016 18:50
Last Modified:15 Dec 2016 18:50

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