Sustainable Oxygen Reduction Catalyzed by Whole-Cell Electro-Mutualism

The oxygen reduction reaction (ORR) in living cells efficiently generates energy but is limited for sustainable applications due to inefficient electron transfer across membranes. Here, we report an interspecies cooperative mechanism, termed electro-mutualism, that enables efficient extracellular ORR using an electrotrophic Acinetobacter venetianus RAG-1 (RAG-1) and a non-CO₂-fixing electrotrophic Shewanella oneidensis MR-1 (MR-1), sustained by inorganic carbon supplied via a bicarbonate-CO₂ equilibrium. Under cathodic polarization, RAG-1 assimilates inorganic carbon and secretes lactate using electrode-derived electrons, which fuels MR-1. In turn, MR-1 releases flavins that interact with the RnfB complex of RAG-1, thereby accelerating the transmembrane electron transfer. This electro-mutualistic cooperation achieves, to our knowledge, the highest reported whole-cell ORR current density (20.9 A/m²) under O₂-aerated, neutral-pH conditions, outperforming benchmark Pt/C and laccase cathodes evaluated under identical conditions. The universality of electro-mutualism is further supported by replacing MR-1 with Bacillus subtilis and is predicted to extend across proteobacteria, firmicutes, and actinobacteria. Electro-mutualism thus provides a metal-free, genetically unmodified catalytic strategy for green energy conversion.