PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli

Abstract Background Exoribonucleases are crucial for RNA degradation in Escherichia coli but the roles of RNase R and PNPase and their potential overlap in stationary phase are not well characterized. Here, we used a genome-wide approach to determine how RNase R and PNPase affect the mRNA half-lives...

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Main Authors: Clémentine Dressaire, Vânia Pobre, Sandrine Laguerre, Laurence Girbal, Cecilia Maria Arraiano, Muriel Cocaign-Bousquet
Format: Article
Language:English
Published: BMC 2018-11-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-018-5259-8
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spelling doaj-2fd3eed0be0c45e7969770ff1852388b2020-11-24T22:04:58ZengBMCBMC Genomics1471-21642018-11-0119111310.1186/s12864-018-5259-8PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coliClémentine Dressaire0Vânia Pobre1Sandrine Laguerre2Laurence Girbal3Cecilia Maria Arraiano4Muriel Cocaign-Bousquet5Instituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de LisboaInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de LisboaLISBP, Université de Toulouse, CNRS, INRA, INSALISBP, Université de Toulouse, CNRS, INRA, INSAInstituto de Tecnologia Química e Biológica António Xavier, Universidade Nova de LisboaLISBP, Université de Toulouse, CNRS, INRA, INSAAbstract Background Exoribonucleases are crucial for RNA degradation in Escherichia coli but the roles of RNase R and PNPase and their potential overlap in stationary phase are not well characterized. Here, we used a genome-wide approach to determine how RNase R and PNPase affect the mRNA half-lives in the stationary phase. The genome-wide mRNA half-lives were determined by a dynamic analysis of transcriptomes after transcription arrest. We have combined the analysis of mRNA half-lives with the steady-state concentrations (transcriptome) to provide an integrated overview of the in vivo activity of these exoribonucleases at the genome-scale. Results The values of mRNA half-lives demonstrated that the mRNAs are very stable in the stationary phase and that the deletion of RNase R or PNPase caused only a limited mRNA stabilization. Intriguingly the absence of PNPase provoked also the destabilization of many mRNAs. These changes in mRNA half-lives in the PNPase deletion strain were associated with a massive reorganization of mRNA levels and also variation in several ncRNA concentrations. Finally, the in vivo activity of the degradation machinery was found frequently saturated by mRNAs in the PNPase mutant unlike in the RNase R mutant, suggesting that the degradation activity is limited by the deletion of PNPase but not by the deletion of RNase R. Conclusions This work had identified PNPase as a central player associated with mRNA degradation in stationary phase.http://link.springer.com/article/10.1186/s12864-018-5259-8RNA decayPNPaseRNase RE. coliTranscriptomeGene expression regulation
collection DOAJ
language English
format Article
sources DOAJ
author Clémentine Dressaire
Vânia Pobre
Sandrine Laguerre
Laurence Girbal
Cecilia Maria Arraiano
Muriel Cocaign-Bousquet
spellingShingle Clémentine Dressaire
Vânia Pobre
Sandrine Laguerre
Laurence Girbal
Cecilia Maria Arraiano
Muriel Cocaign-Bousquet
PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
BMC Genomics
RNA decay
PNPase
RNase R
E. coli
Transcriptome
Gene expression regulation
author_facet Clémentine Dressaire
Vânia Pobre
Sandrine Laguerre
Laurence Girbal
Cecilia Maria Arraiano
Muriel Cocaign-Bousquet
author_sort Clémentine Dressaire
title PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
title_short PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
title_full PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
title_fullStr PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
title_full_unstemmed PNPase is involved in the coordination of mRNA degradation and expression in stationary phase cells of Escherichia coli
title_sort pnpase is involved in the coordination of mrna degradation and expression in stationary phase cells of escherichia coli
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2018-11-01
description Abstract Background Exoribonucleases are crucial for RNA degradation in Escherichia coli but the roles of RNase R and PNPase and their potential overlap in stationary phase are not well characterized. Here, we used a genome-wide approach to determine how RNase R and PNPase affect the mRNA half-lives in the stationary phase. The genome-wide mRNA half-lives were determined by a dynamic analysis of transcriptomes after transcription arrest. We have combined the analysis of mRNA half-lives with the steady-state concentrations (transcriptome) to provide an integrated overview of the in vivo activity of these exoribonucleases at the genome-scale. Results The values of mRNA half-lives demonstrated that the mRNAs are very stable in the stationary phase and that the deletion of RNase R or PNPase caused only a limited mRNA stabilization. Intriguingly the absence of PNPase provoked also the destabilization of many mRNAs. These changes in mRNA half-lives in the PNPase deletion strain were associated with a massive reorganization of mRNA levels and also variation in several ncRNA concentrations. Finally, the in vivo activity of the degradation machinery was found frequently saturated by mRNAs in the PNPase mutant unlike in the RNase R mutant, suggesting that the degradation activity is limited by the deletion of PNPase but not by the deletion of RNase R. Conclusions This work had identified PNPase as a central player associated with mRNA degradation in stationary phase.
topic RNA decay
PNPase
RNase R
E. coli
Transcriptome
Gene expression regulation
url http://link.springer.com/article/10.1186/s12864-018-5259-8
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