Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria.
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.
Max-Planck Institute for Marine Microbiology, 28359 Bremen, Germany.|MARUM, Center for Marine Environmental Sciences, University Bremen, 28359 Bremen, Germany.
Gunter
G
Wegener
Max-Planck Institute for Marine Microbiology, 28359 Bremen, Germany.
Viola
V
Krukenberg
Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany.
Dietmar
D
Riedel
Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, 27570 Bremerhaven, Germany.|Center for Biotechnology, Bielefeld University, 33615 Bielefeld, Germany.
Halina E
HE
Tegetmeyer
Max-Planck Institute for Marine Microbiology, 28359 Bremen, Germany.|MARUM, Center for Marine Environmental Sciences, University Bremen, 28359 Bremen, Germany.|Alfred Wegener Institute Helmholtz Center for Polar and Marine Research, 27570 Bremerhaven, Germany.
Antje
A
Boetius
D000693:Anaerobiosis; D001105:Archaea / Q000378:metabolism*; D001419:Bacteria / Q000378:metabolism*; D003580:Cytochromes / Q000378:metabolism; D004579:Electron Transport; D010861:Fimbriae, Bacterial / Q000378:metabolism; D019015:Geologic Sediments / Q000382:microbiology; D006418:Heme / Q000378:metabolism; D006859:Hydrogen / Q000378:metabolism; D060086:Hydrothermal Vents / Q000382:microbiology; D008697:Methane / Q000378:metabolism*; D064307:Microbiota / Q000502:physiology; D008969:Molecular Sequence Data; D009792:Oceans and Seas; D013431:Sulfates / Q000378:metabolism; D013559:Symbiosis; D013696:Temperature
D003580:Cytochromes; D013431:Sulfates; D006418:Heme; D006859:Hydrogen; D008697:Methane