The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels

ABSTRACT In the bacterium Escherichia coli, the posttranscriptional regulatory system Csr was postulated to influence the transition from glycolysis to gluconeogenesis. Here, we explored the role of the Csr system in the glucose-acetate transition as a model of the glycolysis-to-gluconeogenesis swit...

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Autores principales: Manon Morin, Delphine Ropers, Eugenio Cinquemani, Jean-Charles Portais, Brice Enjalbert, Muriel Cocaign-Bousquet
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:7a724078952d4022b39c69877387f4502021-11-15T15:51:50ZThe Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels10.1128/mBio.01628-172150-7511https://doaj.org/article/7a724078952d4022b39c69877387f4502017-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01628-17https://doaj.org/toc/2150-7511ABSTRACT In the bacterium Escherichia coli, the posttranscriptional regulatory system Csr was postulated to influence the transition from glycolysis to gluconeogenesis. Here, we explored the role of the Csr system in the glucose-acetate transition as a model of the glycolysis-to-gluconeogenesis switch. Mutations in the Csr system influence the reorganization of gene expression after glucose exhaustion and disturb the timing of acetate reconsumption after glucose exhaustion. Analysis of metabolite concentrations during the transition revealed that the Csr system has a major effect on the energy levels of the cells after glucose exhaustion. This influence was demonstrated to result directly from the effect of the Csr system on glycogen accumulation. Mutation in glycogen metabolism was also demonstrated to hinder metabolic adaptation after glucose exhaustion because of insufficient energy. This work explains how the Csr system influences E. coli fitness during the glycolysis-gluconeogenesis switch and demonstrates the role of glycogen in maintenance of the energy charge during metabolic adaptation. IMPORTANCE Glycogen is a polysaccharide and the main storage form of glucose from bacteria such as Escherichia coli to yeasts and mammals. Although its function as a sugar reserve in mammals is well documented, the role of glycogen in bacteria is not as clear. By studying the role of posttranscriptional regulation during metabolic adaptation, for the first time, we demonstrate the role of sugar reserve played by glycogen in E. coli. Indeed, glycogen not only makes it possible to maintain sufficient energy during metabolic transitions but is also the key component in the capacity of cells to resume growth. Since the essential posttranscriptional regulatory system Csr is a major regulator of glycogen accumulation, this work also sheds light on the central role of posttranscriptional regulation in metabolic adaptation.Manon MorinDelphine RopersEugenio CinquemaniJean-Charles PortaisBrice EnjalbertMuriel Cocaign-BousquetAmerican Society for MicrobiologyarticleCsr systemcarbon metabolismEscherichia coliglycogenMicrobiologyQR1-502ENmBio, Vol 8, Iss 5 (2017)
institution DOAJ
collection DOAJ
language EN
topic Csr system
carbon metabolism
Escherichia coli
glycogen
Microbiology
QR1-502
spellingShingle Csr system
carbon metabolism
Escherichia coli
glycogen
Microbiology
QR1-502
Manon Morin
Delphine Ropers
Eugenio Cinquemani
Jean-Charles Portais
Brice Enjalbert
Muriel Cocaign-Bousquet
The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
description ABSTRACT In the bacterium Escherichia coli, the posttranscriptional regulatory system Csr was postulated to influence the transition from glycolysis to gluconeogenesis. Here, we explored the role of the Csr system in the glucose-acetate transition as a model of the glycolysis-to-gluconeogenesis switch. Mutations in the Csr system influence the reorganization of gene expression after glucose exhaustion and disturb the timing of acetate reconsumption after glucose exhaustion. Analysis of metabolite concentrations during the transition revealed that the Csr system has a major effect on the energy levels of the cells after glucose exhaustion. This influence was demonstrated to result directly from the effect of the Csr system on glycogen accumulation. Mutation in glycogen metabolism was also demonstrated to hinder metabolic adaptation after glucose exhaustion because of insufficient energy. This work explains how the Csr system influences E. coli fitness during the glycolysis-gluconeogenesis switch and demonstrates the role of glycogen in maintenance of the energy charge during metabolic adaptation. IMPORTANCE Glycogen is a polysaccharide and the main storage form of glucose from bacteria such as Escherichia coli to yeasts and mammals. Although its function as a sugar reserve in mammals is well documented, the role of glycogen in bacteria is not as clear. By studying the role of posttranscriptional regulation during metabolic adaptation, for the first time, we demonstrate the role of sugar reserve played by glycogen in E. coli. Indeed, glycogen not only makes it possible to maintain sufficient energy during metabolic transitions but is also the key component in the capacity of cells to resume growth. Since the essential posttranscriptional regulatory system Csr is a major regulator of glycogen accumulation, this work also sheds light on the central role of posttranscriptional regulation in metabolic adaptation.
format article
author Manon Morin
Delphine Ropers
Eugenio Cinquemani
Jean-Charles Portais
Brice Enjalbert
Muriel Cocaign-Bousquet
author_facet Manon Morin
Delphine Ropers
Eugenio Cinquemani
Jean-Charles Portais
Brice Enjalbert
Muriel Cocaign-Bousquet
author_sort Manon Morin
title The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
title_short The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
title_full The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
title_fullStr The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
title_full_unstemmed The Csr System Regulates <italic toggle="yes">Escherichia coli</italic> Fitness by Controlling Glycogen Accumulation and Energy Levels
title_sort csr system regulates <italic toggle="yes">escherichia coli</italic> fitness by controlling glycogen accumulation and energy levels
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/7a724078952d4022b39c69877387f450
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