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Structural and functional characterization of the intracellular filament-forming nitrite oxidoreductase multiprotein complex.

ABSTRACT: Nitrate is an abundant nutrient and electron acceptor throughout Earth's biosphere. Virtually all nitrate in nature is produced by the oxidation of nitrite by the nitrite oxidoreductase (NXR) multiprotein complex. NXR is a crucial enzyme in the global biological nitrogen cycle, and is found in nitrite-oxidizing bacteria (including comammox organisms), which generate the bulk of the nitrate in the environment, and in anaerobic ammonium-oxidizing (anammox) bacteria which produce half of the dinitrogen gas in our atmosphere. However, despite its central role in biology and decades of intense study, no structural information on NXR is available. Here, we present a structural and biochemical analysis of the NXR from the anammox bacterium Kuenenia stuttgartiensis, integrating X-ray crystallography, cryo-electron tomography, helical reconstruction cryo-electron microscopy, interaction and reconstitution studies and enzyme kinetics. We find that NXR catalyses both nitrite oxidation and nitrate reduction, and show that in the cell, NXR is arranged in tubules several hundred nanometres long. We reveal the tubule architecture and show that tubule formation is induced by a previously unidentified, haem-containing subunit, NXR-T. The results also reveal unexpected features in the active site of the enzyme, an unusual cofactor coordination in the protein's electron transport chain, and elucidate the electron transfer pathways within the complex.

SUBMITTER: Chicano TM

PROVIDER: S-EPMC8387239 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Structural and functional characterization of the intracellular filament-forming nitrite oxidoreductase multiprotein complex.

Chicano Tadeo Moreno TM Dietrich Lea L de Almeida Naomi M NM Akram Mohd M Hartmann Elisabeth E Leidreiter Franziska F Leopoldus Daniel D Mueller Melanie M Sánchez Ricardo R Nuijten Guylaine H L GHL Reimann Joachim J Seifert Kerstin-Anikó KA Schlichting Ilme I van Niftrik Laura L Jetten Mike S M MSM Dietl Andreas A Kartal Boran B Parey Kristian K Barends Thomas R M TRM

Nature microbiology 20210715 9

Nitrate is an abundant nutrient and electron acceptor throughout Earth's biosphere. Virtually all nitrate in nature is produced by the oxidation of nitrite by the nitrite oxidoreductase (NXR) multiprotein complex. NXR is a crucial enzyme in the global biological nitrogen cycle, and is found in nitrite-oxidizing bacteria (including comammox organisms), which generate the bulk of the nitrate in the environment, and in anaerobic ammonium-oxidizing (anammox) bacteria which produce half of the dinitr ...[more]

PMID: 34267357

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Dataset Information

Structural and functional characterization of the intracellular filament-forming nitrite oxidoreductase multiprotein complex.

Publications

Structural and functional characterization of the intracellular filament-forming nitrite oxidoreductase multiprotein complex.

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