Intercellular Wiring Enables Electron Transfer Between Methanotrophic Archaea and Bacteria

Nature. 2015 Oct 22;526(7574):587-90. doi: 10.1038/nature15733.

Abstract

The anaerobic oxidation of methane (AOM) with sulfate controls the emission of the greenhouse gas methane from the ocean floor. In marine sediments, AOM is performed by dual-species consortia of anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB) inhabiting the methane-sulfate transition zone. The biochemical pathways and biological adaptations enabling this globally relevant process are not fully understood. Here we study the syntrophic interaction in thermophilic AOM (TAOM) between ANME-1 archaea and their consortium partner SRB HotSeep-1 (ref. 6) at 60 °C to test the hypothesis of a direct interspecies exchange of electrons. The activity of TAOM consortia was compared to the first ANME-free culture of an AOM partner bacterium that grows using hydrogen as the sole electron donor. The thermophilic ANME-1 do not produce sufficient hydrogen to sustain the observed growth of the HotSeep-1 partner. Enhancing the growth of the HotSeep-1 partner by hydrogen addition represses methane oxidation and the metabolic activity of ANME-1. Further supporting the hypothesis of direct electron transfer between the partners, we observe that under TAOM conditions, both ANME and the HotSeep-1 bacteria overexpress genes for extracellular cytochrome production and form cell-to-cell connections that resemble the nanowire structures responsible for interspecies electron transfer between syntrophic consortia of Geobacter. HotSeep-1 highly expresses genes for pili production only during consortial growth using methane, and the nanowire-like structures are absent in HotSeep-1 cells isolated with hydrogen. These observations suggest that direct electron transfer is a principal mechanism in TAOM, which may also explain the enigmatic functioning and specificity of other methanotrophic ANME-SRB consortia.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anaerobiosis
  • Archaea / metabolism*
  • Bacteria / metabolism*
  • Cytochromes / metabolism
  • Electron Transport
  • Fimbriae, Bacterial / metabolism
  • Geologic Sediments / microbiology
  • Heme / metabolism
  • Hydrogen / metabolism
  • Hydrothermal Vents / microbiology
  • Methane / metabolism*
  • Microbiota / physiology
  • Molecular Sequence Data
  • Oceans and Seas
  • Sulfates / metabolism
  • Symbiosis
  • Temperature

Substances

  • Cytochromes
  • Sulfates
  • Heme
  • Hydrogen
  • Methane

Associated data

  • BioProject/PRJNA276404
  • BioProject/PRJNA286178
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