The Csr System Regulates Escherichia coli Fitness by Controlling Glycogen Accumulation and Energy Levels.

Manon Morin,Brice Enjalbert,Muriel Cocaign-Bousquet,Eugenio Cinquemani,Jean-Charles Portais,Delphine Ropers

doi:10.1128/mbio.01628-17

Abstract

ABSTRACTIn 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.

Highlights

In the bacterium Escherichia coli, the posttranscriptional regulatory system carbon storage regulator (Csr) was postulated to influence the transition from glycolysis to gluconeogenesis
The Csr system was recently demonstrated to be a major controller of upper glycolysis fluxes [16], but its involvement in metabolic adaptation is less clear in the literature
We showed that gene expression in the central carbon metabolism (CCM) did not present strong discrepancies between the Csr system mutants during the acetate consumption phase, in deep contrast to the situation during glucose consumption

Summary

Introduction

In the bacterium Escherichia coli, the posttranscriptional regulatory system Csr was postulated to influence the transition from glycolysis to gluconeogenesis. We explored the role of the Csr system in the glucose-acetate transition as a model of the glycolysis-to-gluconeogenesis switch. 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. 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. We demonstrate the important role of the Csr system during this metabolic transition through its control of glycogen accumulation and cell energy homeostasis

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Conclusion