Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>

ABSTRACT Bacteria have to continuously adjust to nutrient fluctuations from favorable to less-favorable conditions and in response to carbon starvation. The glucose-acetate transition followed by carbon starvation is representative of such carbon fluctuations observed in Escherichia coli in many env...

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Autores principales:	Manon Morin, Brice Enjalbert, Delphine Ropers, Laurence Girbal, Muriel Cocaign-Bousquet
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	mRNA stability Escherichia coli carbon starvation metabolic transition posttranscriptional regulation transcriptomic Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/cd3cf39d09b14f78a866c09d8e4baa8e
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spelling	oai:doaj.org-article:cd3cf39d09b14f78a866c09d8e4baa8e2021-11-15T15:30:15ZGenomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>10.1128/mSphere.00276-202379-5042https://doaj.org/article/cd3cf39d09b14f78a866c09d8e4baa8e2020-06-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00276-20https://doaj.org/toc/2379-5042ABSTRACT Bacteria have to continuously adjust to nutrient fluctuations from favorable to less-favorable conditions and in response to carbon starvation. The glucose-acetate transition followed by carbon starvation is representative of such carbon fluctuations observed in Escherichia coli in many environments. Regulation of gene expression through fine-tuning of mRNA pools constitutes one of the regulation levels required for such a metabolic adaptation. It results from both mRNA transcription and degradation controls. However, the contribution of transcript stability regulation in gene expression is poorly characterized. Using combined transcriptome and mRNA decay analyses, we investigated (i) how transcript stability changes in E. coli during the glucose-acetate-starvation transition and (ii) if these changes contribute to gene expression changes. Our work highlights that transcript stability increases with carbon depletion. Most of the stabilization occurs at the glucose-acetate transition when glucose is exhausted, and then stabilized mRNAs remain stable during acetate consumption and carbon starvation. Meanwhile, expression of most genes is downregulated and we observed three times less gene expression upregulation. Using control analysis theory on 375 genes, we show that most of gene expression regulation is driven by changes in transcription. Although mRNA stabilization is not the controlling phenomenon, it contributes to the emphasis or attenuation of transcriptional regulation. Moreover, upregulation of 18 genes (33% of our studied upregulated set) is governed mainly by transcript stabilization. Because these genes are associated with responses to nutrient changes and stress, this underscores a potentially important role of posttranscriptional regulation in bacterial responses to nutrient starvation. IMPORTANCE The ability to rapidly respond to changing nutrients is crucial for E. coli to survive in many environments, including the gut. Reorganization of gene expression is the first step used by bacteria to adjust their metabolism accordingly. It involves fine-tuning of both transcription (transcriptional regulation) and mRNA stability (posttranscriptional regulation). While the forms of transcriptional regulation have been extensively studied, the role of mRNA stability during a metabolic switch is poorly understood. Investigating E. coli genomewide transcriptome and mRNA stability during metabolic transitions representative of the carbon source fluctuations in many environments, we have documented the role of mRNA stability in the response to nutrient changes. mRNAs are globally stabilized during carbon depletion. For a few genes, this leads directly to expression upregulation. As these genes are regulators of stress responses and metabolism, our work sheds new light on the likely importance of posttranscriptional regulations in response to environmental stress.Manon MorinBrice EnjalbertDelphine RopersLaurence GirbalMuriel Cocaign-BousquetAmerican Society for MicrobiologyarticlemRNA stabilityEscherichia colicarbon starvationmetabolic transitionposttranscriptional regulationtranscriptomicMicrobiologyQR1-502ENmSphere, Vol 5, Iss 3 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	mRNA stability Escherichia coli carbon starvation metabolic transition posttranscriptional regulation transcriptomic Microbiology QR1-502
spellingShingle	mRNA stability Escherichia coli carbon starvation metabolic transition posttranscriptional regulation transcriptomic Microbiology QR1-502 Manon Morin Brice Enjalbert Delphine Ropers Laurence Girbal Muriel Cocaign-Bousquet Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
description	ABSTRACT Bacteria have to continuously adjust to nutrient fluctuations from favorable to less-favorable conditions and in response to carbon starvation. The glucose-acetate transition followed by carbon starvation is representative of such carbon fluctuations observed in Escherichia coli in many environments. Regulation of gene expression through fine-tuning of mRNA pools constitutes one of the regulation levels required for such a metabolic adaptation. It results from both mRNA transcription and degradation controls. However, the contribution of transcript stability regulation in gene expression is poorly characterized. Using combined transcriptome and mRNA decay analyses, we investigated (i) how transcript stability changes in E. coli during the glucose-acetate-starvation transition and (ii) if these changes contribute to gene expression changes. Our work highlights that transcript stability increases with carbon depletion. Most of the stabilization occurs at the glucose-acetate transition when glucose is exhausted, and then stabilized mRNAs remain stable during acetate consumption and carbon starvation. Meanwhile, expression of most genes is downregulated and we observed three times less gene expression upregulation. Using control analysis theory on 375 genes, we show that most of gene expression regulation is driven by changes in transcription. Although mRNA stabilization is not the controlling phenomenon, it contributes to the emphasis or attenuation of transcriptional regulation. Moreover, upregulation of 18 genes (33% of our studied upregulated set) is governed mainly by transcript stabilization. Because these genes are associated with responses to nutrient changes and stress, this underscores a potentially important role of posttranscriptional regulation in bacterial responses to nutrient starvation. IMPORTANCE The ability to rapidly respond to changing nutrients is crucial for E. coli to survive in many environments, including the gut. Reorganization of gene expression is the first step used by bacteria to adjust their metabolism accordingly. It involves fine-tuning of both transcription (transcriptional regulation) and mRNA stability (posttranscriptional regulation). While the forms of transcriptional regulation have been extensively studied, the role of mRNA stability during a metabolic switch is poorly understood. Investigating E. coli genomewide transcriptome and mRNA stability during metabolic transitions representative of the carbon source fluctuations in many environments, we have documented the role of mRNA stability in the response to nutrient changes. mRNAs are globally stabilized during carbon depletion. For a few genes, this leads directly to expression upregulation. As these genes are regulators of stress responses and metabolism, our work sheds new light on the likely importance of posttranscriptional regulations in response to environmental stress.
format	article
author	Manon Morin Brice Enjalbert Delphine Ropers Laurence Girbal Muriel Cocaign-Bousquet
author_facet	Manon Morin Brice Enjalbert Delphine Ropers Laurence Girbal Muriel Cocaign-Bousquet
author_sort	Manon Morin
title	Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
title_short	Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full	Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
title_fullStr	Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
title_full_unstemmed	Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>
title_sort	genomewide stabilization of mrna during a “feast-to-famine” growth transition in <named-content content-type="genus-species">escherichia coli</named-content>
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/cd3cf39d09b14f78a866c09d8e4baa8e
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Genomewide Stabilization of mRNA during a “Feast-to-Famine” Growth Transition in <named-content content-type="genus-species">Escherichia coli</named-content>

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