Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803

Cyanobacteria adapt to nitrogen starvation by undergoing chlorosis, a regulated bleaching process that involves the degradation of phycobilisomes, the light-harvesting antennae complexes, and accumulation of glycogen. While this response is well characterized under photoautotrophic conditions, its m...

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Autores: Ortega-Martínez, Pablo, Giner-Lamia, Joaquín, Wey, Laura T, Muro-Pastor, M. Isabel, Florencio, Francisco J., Díaz-Troya, Sandra
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2025
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/411770
Acesso em linha:http://hdl.handle.net/10261/411770
https://api.elsevier.com/content/abstract/scopus_id/105022670723
Access Level:acceso abierto
Palavra-chave:Carbon metabolism
Chlorosis
Cyanobacteria
Nitrogen metabolism
Photomixotrophy
Photosynthesis
photosynthesis
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spelling Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803Ortega-Martínez, PabloGiner-Lamia, JoaquínWey, Laura TMuro-Pastor, M. IsabelFlorencio, Francisco J.Díaz-Troya, SandraCarbon metabolismChlorosisCyanobacteriaNitrogen metabolismPhotomixotrophyPhotosynthesisCyanobacteriaphotosynthesisCyanobacteria adapt to nitrogen starvation by undergoing chlorosis, a regulated bleaching process that involves the degradation of phycobilisomes, the light-harvesting antennae complexes, and accumulation of glycogen. While this response is well characterized under photoautotrophic conditions, its modulation by external organic carbon sources such as glucose remains poorly characterized. Here, we investigated how glucose affects the response to nitrogen deprivation in the model cyanobacterium Synechocystis sp. PCC 6803. Using an integrative approach combining physiological assays, targeted metabolomics, RNA sequencing, chlorophyll fluorescence and absorbance spectroscopy, we studied the underlying regulatory mechanisms, focusing on photosynthetic electron transport. Glucose supplementation prevented bleaching, even when added after nitrogen deprivation symptoms had begun. This effect was associated with excess glycogen accumulation, disrupted carbon partitioning, and buildup of metabolic intermediates, indicating a metabolic overflow. Despite these physiological differences, transcriptomic responses to nitrogen deprivation were largely similar regardless of glucose supplementation, suggesting regulation at the post-transcriptional or metabolic level. Glucose also impaired photosynthetic electron transport by creating a redox bottleneck at the photosystem II (PSII) acceptor side, leading to decreased electron transport to photosystem I (PSI) and oxidation of the P700 pool. These findings suggest that reduction of the P700 acceptor side is required to trigger chlorosis. Our results demonstrate that glucose uncouples nitrogen sensing from the bleaching process by altering photosynthetic electron flow. We propose the existence of a redox-sensitive checkpoint that integrates metabolic state with photosynthetic performance, offering new insights into stress adaptation in cyanobacteria.This work was funded by grants PID2019-104513GB-I00 and PID2022-138317NB-I00 both financed by MCIU/AEI/10.13039/501100011033/‘FEDER Una manera de hacer Europa’ to Francisco J. Florencio and M. Isabel Muro-Pastor, by Junta de Andalucía, Group BIO-0284 to Francisco J. Florencio and by Novo Nordisk Foundation (NNF22OCOO79717) to Laura T.Peer reviewedJohn Wiley & SonsMinisterio de Ciencia, Innovación y Universidades (España)Agencia Estatal de Investigación (España)European CommissionJunta de AndalucíaNovo Nordisk FoundationOrtega-Martínez, Pablo [0000-0001-5508-5636]Giner-Lamia, Joaquín [0000-0003-1553-8295]Wey, Laura T [0000-0003-2345-0699]Muro-Pastor, M. Isabel [0000-0001-7366-7904]Florencio, Francisco J. [0000-0002-2068-7861]Díaz-Troya, Sandra [0000-0002-5878-9062]Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]202520252025info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionapplication/pdfhttp://hdl.handle.net/10261/411770https://api.elsevier.com/content/abstract/scopus_id/105022670723reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-104513GB-I00info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-138317NB-I00The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1111/ppl.70645http://dx.doi.org/10.1111/ppl.70645Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/4117702026-05-22T06:33:51Z
dc.title.none.fl_str_mv Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
title Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
spellingShingle Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
Ortega-Martínez, Pablo
Carbon metabolism
Chlorosis
Cyanobacteria
Nitrogen metabolism
Photomixotrophy
Photosynthesis
Cyanobacteria
photosynthesis
title_short Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
title_full Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
title_fullStr Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
title_full_unstemmed Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
title_sort Glucose Uncouples Nitrogen Sensing From Chlorosis via a Photosynthetic Checkpoint in Synechocystis sp. PCC 6803
dc.creator.none.fl_str_mv Ortega-Martínez, Pablo
Giner-Lamia, Joaquín
Wey, Laura T
Muro-Pastor, M. Isabel
Florencio, Francisco J.
Díaz-Troya, Sandra
author Ortega-Martínez, Pablo
author_facet Ortega-Martínez, Pablo
Giner-Lamia, Joaquín
Wey, Laura T
Muro-Pastor, M. Isabel
Florencio, Francisco J.
Díaz-Troya, Sandra
author_role author
author2 Giner-Lamia, Joaquín
Wey, Laura T
Muro-Pastor, M. Isabel
Florencio, Francisco J.
Díaz-Troya, Sandra
author2_role author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Ciencia, Innovación y Universidades (España)
Agencia Estatal de Investigación (España)
European Commission
Junta de Andalucía
Novo Nordisk Foundation
Ortega-Martínez, Pablo [0000-0001-5508-5636]
Giner-Lamia, Joaquín [0000-0003-1553-8295]
Wey, Laura T [0000-0003-2345-0699]
Muro-Pastor, M. Isabel [0000-0001-7366-7904]
Florencio, Francisco J. [0000-0002-2068-7861]
Díaz-Troya, Sandra [0000-0002-5878-9062]
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
dc.subject.none.fl_str_mv Carbon metabolism
Chlorosis
Cyanobacteria
Nitrogen metabolism
Photomixotrophy
Photosynthesis
Cyanobacteria
photosynthesis
topic Carbon metabolism
Chlorosis
Cyanobacteria
Nitrogen metabolism
Photomixotrophy
Photosynthesis
Cyanobacteria
photosynthesis
description Cyanobacteria adapt to nitrogen starvation by undergoing chlorosis, a regulated bleaching process that involves the degradation of phycobilisomes, the light-harvesting antennae complexes, and accumulation of glycogen. While this response is well characterized under photoautotrophic conditions, its modulation by external organic carbon sources such as glucose remains poorly characterized. Here, we investigated how glucose affects the response to nitrogen deprivation in the model cyanobacterium Synechocystis sp. PCC 6803. Using an integrative approach combining physiological assays, targeted metabolomics, RNA sequencing, chlorophyll fluorescence and absorbance spectroscopy, we studied the underlying regulatory mechanisms, focusing on photosynthetic electron transport. Glucose supplementation prevented bleaching, even when added after nitrogen deprivation symptoms had begun. This effect was associated with excess glycogen accumulation, disrupted carbon partitioning, and buildup of metabolic intermediates, indicating a metabolic overflow. Despite these physiological differences, transcriptomic responses to nitrogen deprivation were largely similar regardless of glucose supplementation, suggesting regulation at the post-transcriptional or metabolic level. Glucose also impaired photosynthetic electron transport by creating a redox bottleneck at the photosystem II (PSII) acceptor side, leading to decreased electron transport to photosystem I (PSI) and oxidation of the P700 pool. These findings suggest that reduction of the P700 acceptor side is required to trigger chlorosis. Our results demonstrate that glucose uncouples nitrogen sensing from the bleaching process by altering photosynthetic electron flow. We propose the existence of a redox-sensitive checkpoint that integrates metabolic state with photosynthetic performance, offering new insights into stress adaptation in cyanobacteria.
publishDate 2025
dc.date.none.fl_str_mv 2025
2025
2025
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/411770
https://api.elsevier.com/content/abstract/scopus_id/105022670723
url http://hdl.handle.net/10261/411770
https://api.elsevier.com/content/abstract/scopus_id/105022670723
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
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info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/PID2019-104513GB-I00
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2021-2023/PID2022-138317NB-I00
The underlying dataset has been published as supplementary material of the article in the publisher platform at DOI 10.1111/ppl.70645
http://dx.doi.org/10.1111/ppl.70645

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publisher.none.fl_str_mv John Wiley & Sons
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