Light-independent anaerobic microbial oxidation of manganese driven by an electrosyntrophic coculture

Anaerobic microbial manganese oxidation (AMMO) has been considered an ancient biological metabolism for Mn element cycling on Archaean Earth before the presence of oxygen. A light-dependent AMMO was recently observed under strictly anoxic conditions, providing a new proxy for the interpretation of the evolution of oxygenic photosynthesis. However, the feasibility of biotic Mn(II) oxidation in dark geological habitats that must have been abundant remains unknown. Therefore, we discovered that it would be possible to achieve AMMO in a light-independent electrosyntrophic coculture between Rhodopseudomonas palustris and Geobacter metallireducens. Transmission electron microscopy analysis revealed insoluble particle formation in the coculture with Mn(II) addition. X-ray diffraction and X-ray photoelectron spectroscopy analysis verified that these particles were a mixture of MnO₂ and Mn₃O₄. The absence of Mn oxides in either of the monocultures indicated that the Mn(II)-oxidizing activity was induced via electrosyntrophic interactions. Radical quenching and isotopic experiments demonstrated that hydroxyl radicals (•OH) produced from H₂O dissociation by R. palustris in the coculture contributed to Mn(II) oxidation. All these findings suggest a new, symbiosis-dependent and light-independent AMMO route, with potential importance to the evolution of oxygenic photosynthesis and the biogeochemical cycling of manganese on Archaean and modern Earth.