Quinone-heme π-π interactions bridge the biotic-abiotic interface for enhanced methanogenesis

Quinone-based conductive materials promote extracellular electron transfer and methanogenesis during anaerobic digestion, in which the materials mediates the transfer of electrons produced by exoelectrogens to electrotrophic methanogens. However, the electron transfer mechanism between quinone and electrotrophic methanogens at the biotic-abiotic interface remains elusive. In this study, an interface between reduced anthraquinone and Methanosarcina barkeri is established in a microbial electrolysis cell. Biomimetic experiments and characterization of isolated extracellular polymeric substances reveal electronic complementarity between the electron-donating π-system of reduced anthraquinone and the electron-accepting iron-porphyrin ring of heme, which may be released by cell lysis and retained within extracellular polymeric substances. This complementarity may promote π-π interactions that retain redox-active heme and facilitate electron transfer, consistent with lower interfacial resistance (34.3 versus 225 Ω) and 10.6-fold enhancement in cathodic methanogenesis. This study provides insight into quinone-mediated electron transfer at the biotic-abiotic interface and supports the design of electrode materials for bioelectrochemical systems.