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Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea

Skennerton, Connor T. and Chourey, Karuna and Iyer, Ramsunder and Hettich, Robert L. and Tyson, Gene W. and Orphan, Victoria J. and Dubilier, Nicole (2017) Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. mBio, 8 (4). Art. No. e00530-17. ISSN 2150-7511. PMCID PMC5539420. http://resolver.caltech.edu/CaltechAUTHORS:20170807-095231730

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Abstract

The anaerobic oxidation of methane by anaerobic methanotrophic (ANME) archaea in syntrophic partnership with deltaproteobacterial sulfate-reducing bacteria (SRB) is the primary mechanism for methane removal in ocean sediments. The mechanism of their syntrophy has been the subject of much research as traditional intermediate compounds, such as hydrogen and formate, failed to decouple the partners. Recent findings have indicated the potential for extracellular electron transfer from ANME archaea to SRB, though it is unclear how extracellular electrons are integrated into the metabolism of the SRB partner. We used metagenomics to reconstruct eight genomes from the globally distributed SEEP-SRB1 clade of ANME partner bacteria to determine what genomic features are required for syntrophy. The SEEP-SRB1 genomes contain large multiheme cytochromes that were not found in previously described free-living SRB and also lack periplasmic hydrogenases that may prevent an independent lifestyle without an extracellular source of electrons from ANME archaea. Metaproteomics revealed the expression of these cytochromes at in situ methane seep sediments from three sites along the Pacific coast of the United States. Phylogenetic analysis showed that these cytochromes appear to have been horizontally transferred from metal-respiring members of the Deltaproteobacteria such as Geobacter and may allow these syntrophic SRB to accept extracellular electrons in place of other chemical/organic electron donors.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1128/mBio.00530-17DOIArticle
http://mbio.asm.org/content/8/4/e00530-17PublisherArticle
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5539420/PubMed CentralArticle
https://doi.org/10.1128/mBio.01561-17DOIErratum
http://mbio.asm.org/content/8/5/e01561-17ErrataErratum
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5626972PubMed CentralErratum
ORCID:
AuthorORCID
Skennerton, Connor T.0000-0003-1320-4873
Orphan, Victoria J.0000-0002-5374-6178
Dubilier, Nicole0000-0002-9394-825X
Additional Information:© 2017 Skennerton et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license. Received 31 March 2017; Accepted 28 June 2017; Published 1 August 2017. We thank C. Titus Brown and Lisa Cohen for assistance with sequencing the samples from the Santa Monica Mounds. G.W.T. acknowledges support by the University of Queensland Vice-Chancellor's Research Focused Fellowship. This work was funded by the Gordon and Betty Moore Foundation through grant GBMF3780 (to V.J.O.); the US Department of Energy, Office of Science, Office of Biological Environmental Research, under award numbers DE-SC0003940 and DE-SC0010574 (to V.J.O.); and the National Science Foundation’s Center for Dark Energy Biosphere Investigations (C-DEBI) under award number OCE-0939564 (to V.J.O.). This is contribution number 374. This work was funded by the Gordon and Betty Moore Foundation through grant GBMF3780 (to V.J.O.); the US Department of Energy, Office of Science, Office of Biological Environmental Research, under award numbers DE-SC0003940 and DE-SC0010574 (to V.J.O.); and the National Science Foundation’s Center for Dark Energy Biosphere Investigations (C-DEBI) under award number OCE-0939564 (to V.J.O.). Data availability: Raw sequencing data, metagenomic assemblies, and draft genome sequences are available under NCBI bioproject identifiers PRJNA326769 and PRJNA290197.
Funders:
Funding AgencyGrant Number
Gordon and Betty Moore FoundationGBMF3780
Department of Energy (DOE)DE-SC0003940
Department of Energy (DOE)DE-SC0010574
NSFOCE-0939564
Subject Keywords:ANME; AOM; anaerobic oxidation of methane; extracellular electron transfer; SEEP-SRB1; methane seeps; multiheme cytochrome; sulfate-reducing bacteria
PubMed Central ID:PMC5539420
Record Number:CaltechAUTHORS:20170807-095231730
Persistent URL:http://resolver.caltech.edu/CaltechAUTHORS:20170807-095231730
Official Citation:Skennerton CT, Chourey K, Iyer R, Hettich RL, Tyson GW, Orphan VJ. 2017. Methane-fueled syntrophy through extracellular electron transfer: uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea. mBio 8:e00530-17. https://doi.org/10.1128/mBio.00530-17
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:79841
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:07 Aug 2017 17:06
Last Modified:09 Oct 2017 17:46

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