Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria

Abstract Glycogen serves as a metabolic sink in cyanobacteria. Glycogen deficiency causes the extracellular release of distinctive metabolites such as pyruvate and 2-oxoglutarate upon nitrogen depletion; however, the mechanism has not been fully elucidated. This study aimed to elucidate the mechanis...

Full description

Bibliographic Details
Main Authors: Yuichi Kato, Ryota Hidese, Mami Matsuda, Ryudo Ohbayashi, Hiroki Ashida, Akihiko Kondo, Tomohisa Hasunuma
Format: Article
Language:English
Published: Nature Portfolio 2024-02-01
Series:Communications Biology
Online Access:https://doi.org/10.1038/s42003-024-05929-9
_version_ 1797273503079071744
author Yuichi Kato
Ryota Hidese
Mami Matsuda
Ryudo Ohbayashi
Hiroki Ashida
Akihiko Kondo
Tomohisa Hasunuma
author_facet Yuichi Kato
Ryota Hidese
Mami Matsuda
Ryudo Ohbayashi
Hiroki Ashida
Akihiko Kondo
Tomohisa Hasunuma
author_sort Yuichi Kato
collection DOAJ
description Abstract Glycogen serves as a metabolic sink in cyanobacteria. Glycogen deficiency causes the extracellular release of distinctive metabolites such as pyruvate and 2-oxoglutarate upon nitrogen depletion; however, the mechanism has not been fully elucidated. This study aimed to elucidate the mechanism of carbon partitioning in glycogen-deficient cyanobacteria. Extracellular and intracellular metabolites in a glycogen-deficient ΔglgC mutant of Synechococcus elongatus PCC 7942 were comprehensively analyzed. In the presence of a nitrogen source, the ΔglgC mutant released extracellular glutamate rather than pyruvate and 2-oxoglutarate, whereas its intracellular glutamate level was lower than that in the wild-type strain. The de novo synthesis of glutamate increased in the ΔglgC mutant, suggesting that glycogen deficiency enhanced carbon partitioning into glutamate and extracellular excretion through an unidentified transport system. This study proposes a model in which glutamate serves as the prime extracellular metabolic sink alternative to glycogen when nitrogen is available.
first_indexed 2024-03-07T14:45:18Z
format Article
id doaj.art-014f918e275f452594e9c39949cd3c15
institution Directory Open Access Journal
issn 2399-3642
language English
last_indexed 2024-03-07T14:45:18Z
publishDate 2024-02-01
publisher Nature Portfolio
record_format Article
series Communications Biology
spelling doaj.art-014f918e275f452594e9c39949cd3c152024-03-05T19:59:51ZengNature PortfolioCommunications Biology2399-36422024-02-01711910.1038/s42003-024-05929-9Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteriaYuichi Kato0Ryota Hidese1Mami Matsuda2Ryudo Ohbayashi3Hiroki Ashida4Akihiko Kondo5Tomohisa Hasunuma6Engineering Biology Research Center, Kobe UniversityEngineering Biology Research Center, Kobe UniversityEngineering Biology Research Center, Kobe UniversityDepartment of Biological Science, Faculty of Sciences, Shizuoka UniversityGraduate School of Human Development and Environment, Kobe UniversityEngineering Biology Research Center, Kobe UniversityEngineering Biology Research Center, Kobe UniversityAbstract Glycogen serves as a metabolic sink in cyanobacteria. Glycogen deficiency causes the extracellular release of distinctive metabolites such as pyruvate and 2-oxoglutarate upon nitrogen depletion; however, the mechanism has not been fully elucidated. This study aimed to elucidate the mechanism of carbon partitioning in glycogen-deficient cyanobacteria. Extracellular and intracellular metabolites in a glycogen-deficient ΔglgC mutant of Synechococcus elongatus PCC 7942 were comprehensively analyzed. In the presence of a nitrogen source, the ΔglgC mutant released extracellular glutamate rather than pyruvate and 2-oxoglutarate, whereas its intracellular glutamate level was lower than that in the wild-type strain. The de novo synthesis of glutamate increased in the ΔglgC mutant, suggesting that glycogen deficiency enhanced carbon partitioning into glutamate and extracellular excretion through an unidentified transport system. This study proposes a model in which glutamate serves as the prime extracellular metabolic sink alternative to glycogen when nitrogen is available.https://doi.org/10.1038/s42003-024-05929-9
spellingShingle Yuichi Kato
Ryota Hidese
Mami Matsuda
Ryudo Ohbayashi
Hiroki Ashida
Akihiko Kondo
Tomohisa Hasunuma
Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
Communications Biology
title Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
title_full Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
title_fullStr Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
title_full_unstemmed Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
title_short Glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
title_sort glycogen deficiency enhances carbon partitioning into glutamate for an alternative extracellular metabolic sink in cyanobacteria
url https://doi.org/10.1038/s42003-024-05929-9
work_keys_str_mv AT yuichikato glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT ryotahidese glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT mamimatsuda glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT ryudoohbayashi glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT hirokiashida glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT akihikokondo glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria
AT tomohisahasunuma glycogendeficiencyenhancescarbonpartitioningintoglutamateforanalternativeextracellularmetabolicsinkincyanobacteria