Accelerating anaerobic oxidation of methane coupled with extracellular electron transfer to electrodes via magnetite stimulating membrane-bound proteins of anaerobic methanotrophic (ANME) archaea/methanogens

Methane-dependent bioelectrochemcial systems (BESs) have been recently considered as a promising approach for mitigating methane emission, energy harvesting as well as water environment remediation. However, the mechanisms of extracellular electron transfer (EET) from anaerobic methanotrophic (ANME) archaea/methanogens to electrodes are still poorly understood, which limits the further improvement of methane oxidation and current generation. The study presented here showed that, in the presence of magnetite, anodic biofilms primarily comprised of ANME archaea/methanogens were highly conductive, compared to that without magnetite. Further examination with scanning electrochemical microscopy and electrochemical Fourier transform infrared spectra found that, anodic biofilms with magnetite were redox-based conductive, with a higher concentration of redox-active proteins displayed on their surface than that without magnetite. Metagenomic analysis showed that, the difference in the abundance of genes encoding the cytochrome c (CYC)-like proteins in the anodic biofilms with or without magnetite was not significant. However, magnetite specially increased the abundance of genes encoding the membrane-bound proteins, Rnf, and periplasmic heterodisulfide reductase, HdrABC, contained in ANME archaea/methanogens, providing a possibility that magnetite sped up methane oxidation as well as electron transfer from inner membrane to outer membrane in AOM coupled with EET to electrodes. As a result, the current density in methane-dependent BES with magnetite was increased by approximately 6-9 folds.

Automated summary

Methane-dependent bioelectrochemical systems (BESs) show promise for mitigating methane emission, energy harvesting, and water environment remediation. However, the mechanisms of electron transfer from anaerobic methanotrophic (ANME) archaea/methanogens to electrodes are still poorly understood. This study found that magnetite increased the conductivity and presence of redox-active proteins in anodic biofilms primarily composed of ANME archaea/methanogens. Metagenomic analysis revealed that magnetite specifically increased the abundance of genes encoding membrane-bound proteins, which may accelerate methane oxidation and electron transfer in BESs. As a result, the current density in methane-dependent BESs with magnetite was significantly increased.