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Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae

Leu, Andy O. and Cai, Chen and McIlroy, Simon J. and Southam, Gordon and Orphan, Victoria J. and Yuan, Zhiguo and Hu, Shihu and Tyson, Gene W. (2020) Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME Journal, 14 (4). pp. 1030-1041. ISSN 1751-7362. PMCID PMC7082337. https://resolver.caltech.edu/CaltechAUTHORS:20200203-085914271

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Abstract

Anaerobic oxidation of methane (AOM) is a major biological process that reduces global methane emission to the atmosphere. Anaerobic methanotrophic archaea (ANME) mediate this process through the coupling of methane oxidation to different electron acceptors, or in concert with a syntrophic bacterial partner. Recently, ANME belonging to the archaeal family Methanoperedenaceae (formerly known as ANME-2d) were shown to be capable of AOM coupled to nitrate and iron reduction. Here, a freshwater sediment bioreactor fed with methane and Mn(IV) oxides (birnessite) resulted in a microbial community dominated by two novel members of the Methanoperedenaceae, with biochemical profiling of the system demonstrating Mn(IV)-dependent AOM. Genomic and transcriptomic analyses revealed the expression of key genes involved in methane oxidation and several shared multiheme c-type cytochromes (MHCs) that were differentially expressed, indicating the likely use of different extracellular electron transfer pathways. We propose the names “Candidatus Methanoperedens manganicus” and “Candidatus Methanoperedens manganireducens” for the two newly described Methanoperedenaceae species. This study demonstrates the ability of members of the Methanoperedenaceae to couple AOM to the reduction of Mn(IV) oxides, which suggests their potential role in linking methane and manganese cycling in the environment.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1038/s41396-020-0590-xDOIArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/pmc7082337/PubMed CentralArticle
ORCID:
AuthorORCID
Leu, Andy O.0000-0002-9882-9364
Cai, Chen0000-0002-0167-1397
McIlroy, Simon J.0000-0003-3749-8730
Orphan, Victoria J.0000-0002-5374-6178
Yuan, Zhiguo0000-0002-7566-1482
Tyson, Gene W.0000-0001-8559-9427
Additional Information:© 2020 The Author(s). This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/. Received 06 June 2019; Revised 10 December 2019; Accepted 16 January 2020; Published 27 January 2020. We thank Serene Low, Isabelle Krippner, Brian Kemish, and Nicola Angel for library preparation, Illumina sequencing, and computing support and Aharon Oren for providing the species names and etymology. This work was supported by the U.S. Department of Energy’s Office of Biological Environmental Research (DE-SC0016469) and the Australian Research Council (ARC; Discovery project DP170104038). ZY is a recipient of an Australian Laureate Fellowship (FL170100086). AOL was supported by an Australian Postgraduate Award. CC was supported by The University of Queensland International Scholarship and a China Scholarship Council Scholarship. S.H. was supported by an Advanced Queensland Research Fellowship. GWT was supported by an Australian Research Council Future Fellowship (FT170100070). Data availability: Sequencing data are deposited at the NCBI Sequence Read Archive under accession numbers SAMN10868419-SAMN10868422, SAMN10868423, and SAMN11109471-SAMN11109472. All draft genome nucleotide sequences have been deposited under the NCBI Biosample accession numbers SAMN10872749-SAMN10872769. Author Contributions: These authors contributed equally: Andy O. Leu, Chen Cai. The authors declare that they have no conflict of interest.
Funders:
Funding AgencyGrant Number
Department of Energy (DOE)DE-SC0016469
Australian Research CouncilDP170104038
Australian Research CouncilFL170100086
University of QueenslandUNSPECIFIED
China Scholarship CouncilUNSPECIFIED
Australian Research CouncilFT170100070
Subject Keywords:Biogeochemistry; Environmental microbiology
Issue or Number:4
PubMed Central ID:PMC7082337
Record Number:CaltechAUTHORS:20200203-085914271
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20200203-085914271
Official Citation:Leu, A.O., Cai, C., McIlroy, S.J. et al. Anaerobic methane oxidation coupled to manganese reduction by members of the Methanoperedenaceae. ISME J 14, 1030–1041 (2020). https://doi.org/10.1038/s41396-020-0590-x
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:101051
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:03 Feb 2020 17:10
Last Modified:02 Apr 2020 17:44

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