Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria

Abstract When the supply of inorganic carbon is limiting, photosynthetic cyanobacteria excrete nitrite, a toxic intermediate in the ammonia assimilation pathway from nitrate. It has been hypothesized that the excreted nitrite represents excess nitrogen that cannot be further assimilated due to the m...

Full description

Bibliographic Details
Main Authors: Alexander Kraus, Philipp Spät, Stefan Timm, Amy Wilson, Rhena Schumann, Martin Hagemann, Boris Maček, Wolfgang R. Hess
Format: Article
Language:English
Published: Nature Portfolio 2024-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-46253-4
_version_ 1797274015538085888
author Alexander Kraus
Philipp Spät
Stefan Timm
Amy Wilson
Rhena Schumann
Martin Hagemann
Boris Maček
Wolfgang R. Hess
author_facet Alexander Kraus
Philipp Spät
Stefan Timm
Amy Wilson
Rhena Schumann
Martin Hagemann
Boris Maček
Wolfgang R. Hess
author_sort Alexander Kraus
collection DOAJ
description Abstract When the supply of inorganic carbon is limiting, photosynthetic cyanobacteria excrete nitrite, a toxic intermediate in the ammonia assimilation pathway from nitrate. It has been hypothesized that the excreted nitrite represents excess nitrogen that cannot be further assimilated due to the missing carbon, but the underlying molecular mechanisms are unclear. Here, we identified a protein that interacts with nitrite reductase, regulates nitrogen metabolism and promotes nitrite excretion. The protein, which we named NirP1, is encoded by an unannotated gene that is upregulated under low carbon conditions and controlled by transcription factor NtcA, a central regulator of nitrogen homeostasis. Ectopic overexpression of nirP1 in Synechocystis sp. PCC 6803 resulted in a chlorotic phenotype, delayed growth, severe changes in amino acid pools, and nitrite excretion. Coimmunoprecipitation experiments indicated that NirP1 interacts with nitrite reductase, a central enzyme in the assimilation of ammonia from nitrate/nitrite. Our results reveal that NirP1 is widely conserved in cyanobacteria and plays a crucial role in the coordination of C/N primary metabolism by targeting nitrite reductase.
first_indexed 2024-03-07T14:52:21Z
format Article
id doaj.art-33e27bb261424819a5b818a71cd87619
institution Directory Open Access Journal
issn 2041-1723
language English
last_indexed 2024-03-07T14:52:21Z
publishDate 2024-03-01
publisher Nature Portfolio
record_format Article
series Nature Communications
spelling doaj.art-33e27bb261424819a5b818a71cd876192024-03-05T19:36:07ZengNature PortfolioNature Communications2041-17232024-03-0115111410.1038/s41467-024-46253-4Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteriaAlexander Kraus0Philipp Spät1Stefan Timm2Amy Wilson3Rhena Schumann4Martin Hagemann5Boris Maček6Wolfgang R. Hess7Genetics and Experimental Bioinformatics, Faculty of Biology, Freiburg UniversityDepartment of Quantitative Proteomics, Interfaculty Institute for Cell Biology, University of TübingenPlant Physiology Department, Institute of Biosciences, University of RostockGenetics and Experimental Bioinformatics, Faculty of Biology, Freiburg UniversityBiological Station Zingst, University of RostockPlant Physiology Department, Institute of Biosciences, University of RostockDepartment of Quantitative Proteomics, Interfaculty Institute for Cell Biology, University of TübingenGenetics and Experimental Bioinformatics, Faculty of Biology, Freiburg UniversityAbstract When the supply of inorganic carbon is limiting, photosynthetic cyanobacteria excrete nitrite, a toxic intermediate in the ammonia assimilation pathway from nitrate. It has been hypothesized that the excreted nitrite represents excess nitrogen that cannot be further assimilated due to the missing carbon, but the underlying molecular mechanisms are unclear. Here, we identified a protein that interacts with nitrite reductase, regulates nitrogen metabolism and promotes nitrite excretion. The protein, which we named NirP1, is encoded by an unannotated gene that is upregulated under low carbon conditions and controlled by transcription factor NtcA, a central regulator of nitrogen homeostasis. Ectopic overexpression of nirP1 in Synechocystis sp. PCC 6803 resulted in a chlorotic phenotype, delayed growth, severe changes in amino acid pools, and nitrite excretion. Coimmunoprecipitation experiments indicated that NirP1 interacts with nitrite reductase, a central enzyme in the assimilation of ammonia from nitrate/nitrite. Our results reveal that NirP1 is widely conserved in cyanobacteria and plays a crucial role in the coordination of C/N primary metabolism by targeting nitrite reductase.https://doi.org/10.1038/s41467-024-46253-4
spellingShingle Alexander Kraus
Philipp Spät
Stefan Timm
Amy Wilson
Rhena Schumann
Martin Hagemann
Boris Maček
Wolfgang R. Hess
Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
Nature Communications
title Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
title_full Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
title_fullStr Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
title_full_unstemmed Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
title_short Protein NirP1 regulates nitrite reductase and nitrite excretion in cyanobacteria
title_sort protein nirp1 regulates nitrite reductase and nitrite excretion in cyanobacteria
url https://doi.org/10.1038/s41467-024-46253-4
work_keys_str_mv AT alexanderkraus proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT philippspat proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT stefantimm proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT amywilson proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT rhenaschumann proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT martinhagemann proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT borismacek proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria
AT wolfgangrhess proteinnirp1regulatesnitritereductaseandnitriteexcretionincyanobacteria