Manganese-dependent ammonium oxidation associated with sulfur redox cycling in lake sediments

The release of fixed nitrogen as dinitrogen gas (N2) back to the atmosphere plays a major role in global nitrogen cycling. One major pathway of N2 production is anaerobic ammonium oxidation (anammox). Anammox is often considered a nitrite-dependent process, despite the fact that other electron (e) acceptors such as metal oxides are more abundant in various natural settings. Here we present experimental evidence for a two-step relay process of manganese [Mn(IV)]-dependent ammonium oxidation associated with a functionally novel bacterial lineage in a lake system. We observe that the process proceeds through two steps: ammonium acts as the initial e-donor to reduce sulfate to sulfide, followed by the oxidation of sulfide with Mn(IV) as the terminal e-acceptor. This two-step relay process is associated with Ca. Thiovibrio sp. TH_142, a functionally novel bacterium belonging to the order Desulfobulbales, which relies on reduction of Mn(IV) for energy conservation. From the genome of Ca. Thiovibrio sp. TH_142, we identify genes responsible for manganese reduction (dmsE and mtrB) and sulfide oxidation (tusA, dsrEFH and dsrL). We also identify genes associated with sulfate reduction (sat, aprAB and dsrABC) and a functionally unknown protein structurally similar to hydrazine synthase. These results expand the current view of microbial-mediated ammonium transformations under anoxic conditions, paving the way for understanding the coupled nitrogen, sulfur and manganese cycles in warming, less oxygenated aquatic ecosystems.