Methane production by acetate dismutation stimulated by Shewanella oneidensis and carbon materials: An alternative to classical CO₂ reduction

Methane is a major greenhouse gas responsible of global warming and renewable energy, but the precise contribution of biomethane from microbial decomposition is vague because microbial mechanisms are not fully understood. CO₂ reduction and direct acetate dismutation are two main pathways for biomethane production, accounting for ~1/3 and 2/3 of produced methane in terrestrial ecosystems, respectively. A classical process explaining methane production involves CO₂ reduction by direct interspecies electron transfer (DIET). Herein, we hypothesized that methane could also be produced by direct acetate dismutation by syntrophy between electron-donating Shewanella oneidensis MR-1 and electron-accepting methanogens. We tested the effect of two conducting carbon materials, granular activated carbon and carbon nanotubes, on methane production. The electrical activity was monitored with a microbial fuel cell. We used CH₃F, ¹³C labelling, thermodynamics, DNA analysis and modelling to elucidate the mechanism. Results show that the rate of methane production increased by 29.0% using S. oneidensis MR-1, and by 36.2–40.7% using S. oneidensis MR-1 and conducting materials. ¹³C labelling shows that about 94% of methane is produced by acetate dismutation. Findings further show that acetate dismutation is enhanced by exoelectrogenic activity, thus suggesting that electrons from S. oneidensis MR-1 are used to convert methyl groups into methane. Overall our results disclose DIET-acetate dismutation as an alternative mechanism of biomethane production, which is highly stimulated by carbon-based conductive materials. These findings are of significance for further understanding methanogenic progresses with the involvement of electroactive microorganisms in natural environments and artificial anaerobic systems.