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

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 acceptmore » extracellular electrons in place of other chemical/organic electron donors. Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.« less

Authors:
ORCiD logo [1];  [2];  [3];  [4];  [5];  [1]
  1. California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
  3. Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
  5. Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics. School of Chemistry and Molecular Biosciences
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); Gordon and Betty Moore Foundation (United States); National Science Foundation (NSF)
OSTI Identifier:
1394609
Grant/Contract Number:  
AC05-00OR22725; SC0003940; SC0010574; GBMF3780; OCE-0939564
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
mBio (Online)
Additional Journal Information:
Journal Volume: 8; Journal Issue: 4; Journal ID: ISSN 2150-7511
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; ANME; AOM; anaerobic oxidation of methane; extracellular electron transfer; SEEP-SRB1; methane seeps; multiheme cytochrome; sulfate-reducing bacteria

Citation Formats

Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., and Orphan, Victoria J. Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. United States: N. p., 2017. Web. doi:10.1128/mBio.00530-17.
Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., & Orphan, Victoria J. Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. United States. doi:10.1128/mBio.00530-17.
Skennerton, Connor T., Chourey, Karuna, Iyer, Ramsunder, Hettich, Robert L., Tyson, Gene W., and Orphan, Victoria J. Tue . "Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea". United States. doi:10.1128/mBio.00530-17. https://www.osti.gov/servlets/purl/1394609.
@article{osti_1394609,
title = {Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea},
author = {Skennerton, Connor T. and Chourey, Karuna and Iyer, Ramsunder and Hettich, Robert L. and Tyson, Gene W. and Orphan, Victoria J.},
abstractNote = {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. Some archaea, known as anaerobic methanotrophs, are capable of converting methane into carbon dioxide when they are growing syntopically with sulfate-reducing bacteria. This partnership is the primary mechanism for methane removal in ocean sediments; however, there is still much to learn about how this syntrophy works. Previous studies have failed to identify the metabolic intermediate, such as hydrogen or formate, that is passed between partners. However, recent analysis of methanotrophic archaea has suggested that the syntrophy is formed through direct electron transfer. In this research, we analyzed the genomes of multiple partner bacteria and showed that they also contain the genes necessary to perform extracellular electron transfer, which are absent in related bacteria that do not form syntrophic partnerships with anaerobic methanotrophs. This genomic evidence shows a possible mechanism for direct electron transfer from methanotrophic archaea into the metabolism of the partner bacteria.},
doi = {10.1128/mBio.00530-17},
journal = {mBio (Online)},
issn = {2150-7511},
number = 4,
volume = 8,
place = {United States},
year = {2017},
month = {8}
}

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Cited by: 12 works
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    Works referencing / citing this record:

    Physiology and Distribution of Archaeal Methanotrophs That Couple Anaerobic Oxidation of Methane with Sulfate Reduction
    journal, July 2019

    • Bhattarai, S.; Cassarini, C.; Lens, P. N. L.
    • Microbiology and Molecular Biology Reviews, Vol. 83, Issue 3
    • DOI: 10.1128/mmbr.00074-18