Extracellular RNA drives Electromethanogenesis in a Methanogenic Archaeon

Methanogenic archaea generate two-thirds of Earth’s methane. Some reduce CO ₂ by drawing electrons directly from solid substrates. Yet many, including Methanosarcina barkeri , lack the multiheme cytochromes (MHCs), that drive extracellular electron transfer (EET) in other microbes. Here we show that at growth onset, M. barkeri releases an extracellular nucleic-acid pool dominated by short RNAs (∼80%) that self-assemble into G-quadruplexes (G4) on the cell surface. Addition of synthetic G4-RNA doubles cathodic methane production, whereas nuclease digestion abolishes EET. Neither treatment affected growth on soluble substrates. Thus, G4-RNA forms an electron conduit enabling cathodic EET in this MHC-deficient archaeon. The discovery broadens the inventory of biological wiring and hints that nucleic-acid electronics pre-date protein redox systems, with ramifications for early-Earth metabolism, bioenergy and living electronics.