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Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea.
MBio 2017; 8(4)MBIO

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.IMPORTANCE 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.

Authors+Show Affiliations

Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA.Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA.Genome Science and Technology, University of Tennessee, Knoxville, Tennessee, USA.Chemical Sciences Division, Oak Ridge National Laboratory, Oak Ridge, Tennessee, USA. Genome Science and Technology, University of Tennessee, Knoxville, Tennessee, USA.Australian Centre for Ecogenomics, School of Chemistry and Molecular Biosciences, University of Queensland, Brisbane, Queensland, Australia.Division of Geological and Planetary Sciences, California Institute of Technology, Pasadena, California, USA vorphan@gps.caltech.edu.

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.

Language

eng

PubMed ID

28765215

Citation

Skennerton, Connor T., et al. "Methane-Fueled Syntrophy Through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved Within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea." MBio, vol. 8, no. 4, 2017.
Skennerton CT, Chourey K, Iyer R, et al. Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. MBio. 2017;8(4).
Skennerton, C. T., Chourey, K., Iyer, R., Hettich, R. L., Tyson, G. W., & Orphan, V. J. (2017). Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. MBio, 8(4), doi:10.1128/mBio.00530-17.
Skennerton CT, et al. Methane-Fueled Syntrophy Through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved Within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. MBio. 2017 08 1;8(4) PubMed PMID: 28765215.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Methane-Fueled Syntrophy through Extracellular Electron Transfer: Uncovering the Genomic Traits Conserved within Diverse Bacterial Partners of Anaerobic Methanotrophic Archaea. AU - Skennerton,Connor T, AU - Chourey,Karuna, AU - Iyer,Ramsunder, AU - Hettich,Robert L, AU - Tyson,Gene W, AU - Orphan,Victoria J, Y1 - 2017/08/01/ PY - 2017/8/3/entrez PY - 2017/8/3/pubmed PY - 2018/4/4/medline KW - ANME KW - AOM KW - SEEP-SRB1 KW - anaerobic oxidation of methane KW - extracellular electron transfer KW - methane seeps KW - multiheme cytochrome KW - sulfate-reducing bacteria JF - mBio JO - MBio VL - 8 IS - 4 N2 - 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.IMPORTANCE 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. SN - 2150-7511 UR - https://www.unboundmedicine.com/medline/citation/28765215/Methane_Fueled_Syntrophy_through_Extracellular_Electron_Transfer:_Uncovering_the_Genomic_Traits_Conserved_within_Diverse_Bacterial_Partners_of_Anaerobic_Methanotrophic_Archaea_ L2 - http://mbio.asm.org/cgi/pmidlookup?view=long&pmid=28765215 DB - PRIME DP - Unbound Medicine ER -