Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals

Abstract Uncoupling of biological nitrogen fixation from ammonia assimilation is a prerequisite step for engineering ammonia excretion and improvement of plant-associative nitrogen fixation. In this study, we have identified an amino acid substitution in glutamine synthetase, which provides temperat...

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Main Authors: Yuqian Tang, Debin Qin, Zhexian Tian, Wenxi Chen, Yuanxi Ma, Jilong Wang, Jianguo Yang, Dalai Yan, Ray Dixon, Yi-Ping Wang
Format: Article
Language:English
Published: Nature Portfolio 2023-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-023-43370-4
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author Yuqian Tang
Debin Qin
Zhexian Tian
Wenxi Chen
Yuanxi Ma
Jilong Wang
Jianguo Yang
Dalai Yan
Ray Dixon
Yi-Ping Wang
author_facet Yuqian Tang
Debin Qin
Zhexian Tian
Wenxi Chen
Yuanxi Ma
Jilong Wang
Jianguo Yang
Dalai Yan
Ray Dixon
Yi-Ping Wang
author_sort Yuqian Tang
collection DOAJ
description Abstract Uncoupling of biological nitrogen fixation from ammonia assimilation is a prerequisite step for engineering ammonia excretion and improvement of plant-associative nitrogen fixation. In this study, we have identified an amino acid substitution in glutamine synthetase, which provides temperature sensitive biosynthesis of glutamine, the intracellular metabolic signal of the nitrogen status. As a consequence, negative feedback regulation of genes and enzymes subject to nitrogen regulation, including nitrogenase is thermally controlled, enabling ammonia excretion in engineered Escherichia coli and the plant-associated diazotroph Klebsiella oxytoca at 23 °C, but not at 30 °C. We demonstrate that this temperature profile can be exploited to provide diurnal oscillation of ammonia excretion when variant bacteria are used to inoculate cereal crops. We provide evidence that diurnal temperature variation improves nitrogen donation to the plant because the inoculant bacteria have the ability to recover and proliferate at higher temperatures during the daytime.
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spelling doaj.art-34c960633b2e4097afe0dd21ac335d032023-11-20T09:55:19ZengNature PortfolioNature Communications2041-17232023-11-0114111610.1038/s41467-023-43370-4Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cerealsYuqian Tang0Debin Qin1Zhexian Tian2Wenxi Chen3Yuanxi Ma4Jilong Wang5Jianguo Yang6Dalai Yan7Ray Dixon8Yi-Ping Wang9State Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityDepartment of Microbiology and Immunology, Indiana University School of MedicineDepartment of Molecular Microbiology, John Innes CentreState Key Laboratory of Protein and Plant Gene Research, School of Life Sciences & School of Advanced Agricultural Sciences, Peking UniversityAbstract Uncoupling of biological nitrogen fixation from ammonia assimilation is a prerequisite step for engineering ammonia excretion and improvement of plant-associative nitrogen fixation. In this study, we have identified an amino acid substitution in glutamine synthetase, which provides temperature sensitive biosynthesis of glutamine, the intracellular metabolic signal of the nitrogen status. As a consequence, negative feedback regulation of genes and enzymes subject to nitrogen regulation, including nitrogenase is thermally controlled, enabling ammonia excretion in engineered Escherichia coli and the plant-associated diazotroph Klebsiella oxytoca at 23 °C, but not at 30 °C. We demonstrate that this temperature profile can be exploited to provide diurnal oscillation of ammonia excretion when variant bacteria are used to inoculate cereal crops. We provide evidence that diurnal temperature variation improves nitrogen donation to the plant because the inoculant bacteria have the ability to recover and proliferate at higher temperatures during the daytime.https://doi.org/10.1038/s41467-023-43370-4
spellingShingle Yuqian Tang
Debin Qin
Zhexian Tian
Wenxi Chen
Yuanxi Ma
Jilong Wang
Jianguo Yang
Dalai Yan
Ray Dixon
Yi-Ping Wang
Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
Nature Communications
title Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
title_full Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
title_fullStr Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
title_full_unstemmed Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
title_short Diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
title_sort diurnal switches in diazotrophic lifestyle increase nitrogen contribution to cereals
url https://doi.org/10.1038/s41467-023-43370-4
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