Expanded metabolic versatility of ubiquitous nitrite-oxidizing bacteria from the genus Nitrospira

Abstract

Nitrospira are 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 from Nitrospira moscoviensis representing the ubiquitous Nitrospira lineage II, we identified ecophysiological traits that contribute to the ecological success of Nitrospira. Unexpectedly, N. moscoviensis possesses genes coding for a urease and cleaves urea to ammonia and CO2. Ureolysis was not observed yet in nitrite oxidizers and enables N. moscoviensis to 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 in Nitrospira lenta from 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 allows N. moscoviensis to use formate, with or without concomitant nitrite oxidation, using oxygen, nitrate, or both compounds as terminal electron acceptors. Compared with Nitrospira defluvii from lineage I, N. moscoviensis shares the Nitrospira core 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 of Nitrospira in natural and engineered ecosystems.

Metagenomic analysis of rapid gravity sand filter microbial communities suggests novel physiology ofNitrospiraspp.

“…In addition, it contained NAD+-dependent formate dehydrogenase and formate transporters, suggesting that it could oxidize formate coupled with the reduction of oxygen, nitrate or nitrite under anoxic conditions, as has been observed in other Nitrospira sp. (Koch et al, 2015). Another feature recently found in Nitrospira, which was also encoded in this bin, is urease which is involved in the hydrolysis of urea into ammonia and carbamate (Koch et al, 2015).…”

“…(Koch et al, 2015). Another feature recently found in Nitrospira, which was also encoded in this bin, is urease which is involved in the hydrolysis of urea into ammonia and carbamate (Koch et al, 2015). CG24 contained urease subunits alpha, beta and gamma.…”

Dynamics of Bacterial Community Abundance and Structure in Horizontal Subsurface Flow Wetland Mesocosms Treating Municipal Wastewater

“…For example, in module A, which was positively related to the removal of ammonia, one of the consortium members belonged to the genus Nitrospira, the main nitrite-oxidizer in wastewater treatment plants. Nitrospira species are able to cleave urea to ammonia and CO 2 and couple formate oxidation with nitrate reduction to remain active in anoxia [59]. In addition, this module harbours phylotypes from the genera Pseudomonas and Rhodococcus and the order Sphingobacteriales that are known for their ability to perform heterotrophic nitrification under low oxygen concentrations (<0.3 mg O 2 /L) [60,61].…”

AmoA-targeted polymerase chain reaction primers for the specific detection and quantification of comammoxNitrospirain the environment

“…For co-occurring Nitrospira in WWTPs, niche partitioning based on the preferred nitrite concentrations, on the capability to utilize formate as an alternative substrate, and on the tendency to co-aggregate with AOB has already been demonstrated Gruber-Dorninger et al, 2015). It is tempting to speculate that underlying mechanisms of niche differentiation of comammox Nitrospira could also be different substrate (ammonia) concentration optima and alternative energy metabolisms, such as the oxidation of formate and of hydrogen (Koch et al, , 2015.…”

“…All known comammox organisms belong to Nitrospira sublineage II (Daims et al, 2015;van Kessel et al, 2015;Palomo et al, 2016;Pinto et al, 2016). This sublineage contains also canonical NOB, which lack the genes for ammonia oxidation (Daims et al, 2001;Koch et al, 2015). Moreover, the known comammox Nitrospira do not form a monophyletic clade within Nitrospira lineage II in phylogenies based on 16S rRNA genes or nxrB, the gene encoding subunit beta of the functional key enzyme nitrite oxidoreductase.…”