Methane-fueled syntrophy through extracellular electron transfer: Uncovering the genomic traits conserved within diverse bacterial partners of anaerobic methanotrophic archaea

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

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71 Scopus citations

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.

Original languageEnglish
Article numbere00530-17
JournalmBio
Volume8
Issue number4
DOIs
StatePublished - Jul 1 2017

Funding

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 DESC0010574 (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. 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.

FundersFunder number
National Science Foundation’s Center for Dark Energy Biosphere Investigations
Office of Biological Environmental ResearchDESC0010574, DE-SC0003940
U.S. Department of Energy
Directorate for Geosciences0939564
Gordon and Betty Moore FoundationGBMF3780
Office of Science
Center for Dark Energy Biosphere InvestigationsOCE-0939564
University of Queensland

    Keywords

    • ANME
    • AOM
    • Anaerobic oxidation of methane
    • Extracellular electron transfer
    • Methane seeps
    • Multiheme cytochrome
    • SEEP-SRB1
    • Sulfate-reducing bacteria

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