Manganese is one of the most abundant elements on Earth. The oxidation of manganese has long been theorized(1)-yet has not been demonstrated(2-4)-to fuel the growth of chemolithoautotrophic microorganisms. Here we refine an enrichment culture that exhibits exponential growth dependent on Mn(II) oxidation to a co-culture of two microbial species. Oxidation required viable bacteria at permissive temperatures, which resulted in the generation of small nodules of manganese oxide with which the cells associated. The majority member of the culture-which we designate 'CandidatusManganitrophus noduliformans'-is affiliated to the phylum Nitrospirae (also known as Nitrospirota), but is distantly related to known species ofNitrospiraandLeptospirillum. We isolated the minority member, a betaproteobacterium that does not oxidize Mn(II) alone, and designate itRamlibacter lithotrophicus. Stable-isotope probing revealed(13)CO(2)fixation into cellular biomass that was dependent upon Mn(II) oxidation. Transcriptomic analysis revealed candidate pathways for coupling extracellular manganese oxidation to aerobic energy conservation and autotrophic CO(2)fixation. These findings expand the known diversity of inorganic metabolisms that support life, and complete a biogeochemical energy cycle for manganese(5,6)that may interface with other major global elemental cycles. A co-culture of two newly identified microorganisms-'CandidatusManganitrophus noduliformans' andRamlibacter lithotrophicus-exhibits exponential growth that is dependent on manganese(II) oxidation, demonstrating the viability of this metabolism for supporting life.