Intercellular wiring enables electron transfer between methanotrophic archaea and bacteria.

Area of Science:

• Microbial Ecology
• Biogeochemistry
• Environmental Microbiology

Background:

• Anaerobic oxidation of methane (AOM) by microbial consortia controls methane release from marine sediments.
• The specific mechanisms and biological adaptations driving AOM, particularly in thermophilic conditions, remain unclear.
• AOM is performed by syntrophic partnerships between anaerobic methanotrophic archaea (ANME) and sulfate-reducing bacteria (SRB).

Purpose of the Study:

• To investigate the syntrophic interaction in thermophilic AOM (TAOM) between ANME-1 archaea and SRB HotSeep-1 at 60 °C.
• To test the hypothesis of direct interspecies electron transfer (DIET) as the primary mechanism in TAOM.
• To compare TAOM consortia activity with ANME-free cultures of SRB HotSeep-1 grown on hydrogen.

Main Methods:

• Cultivation of TAOM consortia and ANME-free SRB HotSeep-1.
• Comparative analysis of methane oxidation rates and microbial growth under different conditions (consortial vs. ANME-free).
• Gene expression analysis (overexpression of cytochromes and pili) and microscopic observation of cell-to-cell connections (nanowires).

Main Results:

• Thermophilic ANME-1 archaea do not produce sufficient hydrogen to sustain SRB HotSeep-1 growth.
• Hydrogen addition to SRB HotSeep-1 cultures repressed methane oxidation and ANME-1 activity, suggesting competition or feedback.
• Under TAOM conditions, both ANME and SRB overexpressed genes for extracellular cytochromes and formed nanowire-like structures, indicative of DIET.

Conclusions:

• Direct interspecies electron transfer is a principal mechanism driving thermophilic anaerobic oxidation of methane.
• The formation of cell-to-cell connections and overexpression of extracellular electron transfer components support the DIET hypothesis.
• This mechanism may explain the functioning and specificity of other ANME-SRB consortia involved in methane cycling.