Dissimilatory Nitrate Reduction To Ammonium In The Cable Bacterium Ca. Electronema Sp. GS

Cable bacteria are filamentous Desulfobulbaceae that split the energy-conserving reaction of sulphide oxidation into two half reactions occurring in distinct cells. Cable bacteria can use nitrate, but the reduction pathway is unknown, making it difficult to assess their direct impact on the N-cycle. Here we show that the freshwater cable bacterium Ca. Electronema sp. GS performs dissimilatory nitrate reduction to ammonium (DNRA). 15NO3--amended sediment with Ca. Electronema sp. GS showed higher rates of DNRA and nitrite production than sediment without Ca. Electronema sp. GS. Electron flux from sulphide oxidation, inferred from electric potential measurements, matched the electron flux needed to drive cable bacteria-mediated nitrate reduction. Ca. Electronema sp. GS expressed a complete nap operon for periplasmic nitrate reduction to nitrite, and genes encoding a periplasmic multiheme cytochrome (pMHC), homolog to a pMHC that can catalyse nitrite reduction to ammonium in Ca. Maribeggiatoa. Phylogenetic analysis suggests that the capacity for DNRA was acquired in multiple events through horizontal gene transfer from different organisms, before cable bacteria split into different salinity niches. The architecture of the nitrate reduction system suggests absence of energy conservation through oxidative phosphorylation, indicating that cable bacteria primarily conserve energy through the half reaction of sulfide oxidation.