Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genusNitrospira

Abstract

Nitrospiraare a diverse group of nitrite-oxidizing bacteria and among the environmentally most widespread nitrifiers. However, they remain scarcely studied and mostly uncultured. Based on genomic and experimental data fromNitrospira moscoviensisrepresenting the ubiquitousNitrospiralineage II, we identified ecophysiological traits that contribute to the ecological success ofNitrospira. Unexpectedly,N. moscoviensispossesses genes coding for a urease and cleaves urea to ammonia and CO2. Ureolysis was not observed yet in nitrite oxidizers and enablesN. moscoviensisto supply ammonia oxidizers lacking urease with ammonia from urea, which is fully nitrified by this consortium through reciprocal feeding. The presence of highly similar urease genes inNitrospira lentafrom activated sludge, in metagenomes from soils and freshwater habitats, and of other ureases in marine nitrite oxidizers, suggests a wide distribution of this extended interaction between ammonia and nitrite oxidizers, which enables nitrite-oxidizing bacteria to indirectly use urea as a source of energy. A soluble formate dehydrogenase lends additional ecophysiological flexibility and allowsN. moscoviensisto use formate, with or without concomitant nitrite oxidation, using oxygen, nitrate, or both compounds as terminal electron acceptors. Compared withNitrospira defluviifrom lineage I,N. moscoviensisshares theNitrospiracore metabolism but shows substantial genomic dissimilarity including genes for adaptations to elevated oxygen concentrations. Reciprocal feeding and metabolic versatility, including the participation in different nitrogen cycling processes, likely are key factors for the niche partitioning, the ubiquity, and the high diversity ofNitrospirain natural and engineered ecosystems.