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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.

SUBMITTER: Koch H

PROVIDER: S-EPMC4568715 | biostudies-literature | 2015 Sep

REPOSITORIES: biostudies-literature

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

Koch Hanna H Lücker Sebastian S Albertsen Mads M Kitzinger Katharina K Herbold Craig C Spieck Eva E Nielsen Per Halkjaer PH Wagner Michael M Daims Holger H

Proceedings of the National Academy of Sciences of the United States of America 20150824 36

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. Ure ...[more]

PMID: 26305944

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Project description:Nitrite-oxidizing bacteria are vital players in the global nitrogen cycle that convert nitrite to nitrate during the 2nd step of nitrification. Within this functional guild, the genus Nitrospira is among the most widespread and phylogenetically and physiologically diverse nitrite oxidizers and its members drive nitrite oxidation in many natural and biotechnological ecosystems. Despite their ecological and biotechnological importance, our understanding of Nitrospira’s energy metabolism is still limited. The main bottleneck for a detailed biochemical characterization of Nitrospira is biomass production, since they are slow-growing organisms and fastidious to culture. In this study, we cultured Nitrospira moscoviensis in a continuous stirred tank reactor system (CSTR) allowing constant biomass harvesting. Additionally, this cultivation setup enabled accurate control of physicochemical parameters and thus avoided fluctuating levels of nitrite and accumulation of nitrate. We performed transcriptome analysis and confirmed constant gene expression profiles in the chemostat culture over a period of two weeks. The transcriptomic data supports the predicted core metabolism of N. moscoviensis, including the reductive TCA cycle as a CO2 fixation pathway, the novel bd-like oxidase as terminal oxidase and the octaheme nitrite reductase involved in nitrogen assimilation. Additionally, the expression of multiple copies of respiratory complexes suggests functional differentiation of these copies within the respiratory chain. Transcriptome analysis also suggests a soluble and a membrane-bound gamma subunit as part of the nitrite oxidoreductase (NXR), the enzyme catalyzing nitrite oxidation. Overall, the transcriptome data provided novel insights into the metabolism of Nitrospira supporting the genome-based prediction of key pathways. Moreover, the application of a CSTR to cultivate Nitrospira is an important foundation for future proteomic and biochemical characterizations, which are crucial for a better understanding of canonical and complete nitrifying microorganisms.

Dataset Information

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

Publications

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

Similar Datasets

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