Single-cell metal–phenolic nanocoatings protect strictly anaerobic methanogens for methane production at an atmospheric oxygen level

Abstract

Methanogens are powerful catalysts employed in electrobiological systems that are expected to contribute toward carbon dioxide emission reduction and energy production. However, oxygen generated within electrobiological systems can severely reduce the survival of anaerobic methanogens, thus presenting a bottleneck toward further applications and improvement of electrobiological systems. Herein, we report a single-cell nanocoating strategy, using metal–phenolic networks (MPNs), to protect an anaerobically methanogenic archaeon (i.e., Methanosarcina acetivorans C2A) toward achieving methane production at atmospheric oxygen levels. A tannic acid (TA)–Fe²⁺ complex, a coating precursor, is oxidized to TA–Fe³⁺ species by chemically consuming oxygen molecules, which form a self-assembled nanocoating and thus physically reduce the permeability of oxygen without affecting the utilization of methanol by M. acetivorans. Further, RNA-Seq transcriptomic analysis reveals that the coating can facilitate the conversion of methanol into methyl-coenzyme M, thus reducing the inhibitory effect of oxygen on methanogenesis from methanol. At an atmospheric oxygen level, the MPN coating can improve the viability of M. acetivorans from 5% to 37% and increase methane production by 4.6-fold compared to native M. acetivorans. This work provides an avenue to protect anaerobic methanogens from oxygen damage and maintain their activity in the presence of oxygen, which demonstrates the potential of the MPN coating strategy in other anaerobic applications and energy production.