Ancient transfers of archaeal electrogenic metabolism endowed B-proteobacterial ammonia oxidizers with a survival strategy for oxygen deficiency. Ancient transfers of archaeal electrogenic metabolism endowed B-proteobacterial ammonia oxidizers with a survival strategy for oxygen deficiency

Many aerobic microbes are able to utilize alternative electron acceptors under oxygen-limited conditions. In some cases this is mediated by extracellular electron transfer (or EET), wherein electrons are transferred to extracellular oxidants such as iron oxide and manganese oxide minerals. Here, we show that an ammonia-oxidizer previously known to be strictly aerobic, Nitrosomonas communis, was able to utilize a poised electrode to maintain metabolic activity in anoxic conditions. The presence and activity of multi-heme cytochromes in N. communis suggests EET as the underlying metabolic mechanism. Molecular clock analysis shows that the ancestors of β-proteobacterial ammonia oxidizers appeared after Earth's atmospheric oxygenation when the oxygen levels were >10-4 pO2 (PAL), consistent with aerobic origins. Furthermore, phylogenetic reconciliations of gene and species trees show that the multi-heme c‐type EET proteins in Nitrosomonas and Nitrosospira lineages were acquired by gene transfer from -proteobacteria when the oxygen levels were between 0.1 and 1 pO2 (PAL). These results suggest that β-proteobacterial anaerobic ammonia oxidation via EET evolved during the Proterozoic when oxygen limitation was widespread, but oxidized minerals were abundant.