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

Skennerton, Connor T.; Chourey, Karuna; Iyer, Ramsunder; Hettich, Robert L.; Tyson, Gene W.; Orphan, Victoria J.

doi:10.1128/mBio.00530-17

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

Journal Article · Tue Aug 01 00:00:00 EDT 2017 · mBio (Online)

DOI:https://doi.org/10.1128/mBio.00530-17· OSTI ID:1394609

^[1]; Chourey, Karuna ^[2]; Iyer, Ramsunder ^[3]; Hettich, Robert L. ^[4]; Tyson, Gene W. ^[5]; Orphan, Victoria J. ^[1]

California Inst. of Technology (CalTech), Pasadena, CA (United States). Division of Geological and Planetary Sciences
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division
Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Chemical Sciences Division; Univ. of Tennessee, Knoxville, TN (United States). Genome Science and Technology
Univ. of Queensland, Brisbane, QLD (Australia). Australian Centre for Ecogenomics. School of Chemistry and Molecular Biosciences

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.

View Accepted Manuscript (DOE)

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: Gordon and Betty Moore Foundation (United States); National Science Foundation (NSF) (United States); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: AC05-00OR22725; SC0003940; SC0010574

OSTI ID:: 1394609

Journal Information:: mBio (Online), Journal Name: mBio (Online) Journal Issue: 4 Vol. 8; ISSN 2150-7511

Publisher:: American Society for MicrobiologyCopyright Statement

Country of Publication:: United States

Language:: English

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Physiology and Distribution of Archaeal Methanotrophs That Couple Anaerobic Oxidation of Methane with Sulfate Reduction Bhattarai, S.; Cassarini, C.; Lens, P. N. L. Microbiology and Molecular Biology Reviews, Vol. 83, Issue 3 https://doi.org/10.1128/mmbr.00074-18	journal	July 2019
Extracellular Electron Transfer May Be an Overlooked Contribution to Pelagic Respiration in Humic-Rich Freshwater Lakes He, Shaomei; Lau, Maximilian P.; Linz, Alexandra M. mSphere, Vol. 4, Issue 1 https://doi.org/10.1128/msphere.00436-18	journal	January 2019
Contrasting Pathways for Anaerobic Methane Oxidation in Gulf of Mexico Cold Seep Sediments Vigneron, Adrien; Alsop, Eric B.; Cruaud, Perrine mSystems, Vol. 4, Issue 1 https://doi.org/10.1128/msystems.00091-18	journal	February 2019
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The Carbon-Isotope Record of the Sub-Seafloor Biosphere Meister, Patrick; Reyes, Carolina Geosciences, Vol. 9, Issue 12 https://doi.org/10.3390/geosciences9120507	journal	December 2019

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