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...
Guardado en:
Autores principales: | , , , , , |
---|---|
Formato: | article |
Lenguaje: | EN |
Publicado: |
American Society for Microbiology
2017
|
Materias: | |
Acceso en línea: | https://doaj.org/article/7a724078952d4022b39c69877387f450 |
Etiquetas: |
Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
|
id |
oai:doaj.org-article:7a724078952d4022b39c69877387f450 |
---|---|
record_format |
dspace |
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 |
work_keys_str_mv |
AT manonmorin thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT delphineropers thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT eugeniocinquemani thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT jeancharlesportais thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT briceenjalbert thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT murielcocaignbousquet thecsrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT manonmorin csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT delphineropers csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT eugeniocinquemani csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT jeancharlesportais csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT briceenjalbert csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels AT murielcocaignbousquet csrsystemregulatesitalictoggleyesescherichiacoliitalicfitnessbycontrollingglycogenaccumulationandenergylevels |
_version_ |
1718427346460999680 |