Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Autoren

  • Franziska Mika
  • Susan Busse
  • Alexandra Possling
  • Janine Berkholz
  • Natalia Tschowri
  • Nicole Sommerfeldt
  • Mihaela Pruteanu
  • Regine Hengge

Organisationseinheiten

Externe Organisationen

  • Freie Universität Berlin (FU Berlin)
  • IDT Biologika GmbH
  • National University of Ireland, Cork
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Details

OriginalspracheEnglisch
Seiten (von - bis)51-65
Seitenumfang15
FachzeitschriftMolecular microbiology
Jahrgang84
Ausgabenummer1
PublikationsstatusVeröffentlicht - Apr. 2012

Abstract

RprA is a small regulatory RNA known to weakly affect the translation of σ(S) (RpoS) in Escherichia coli. Here we demonstrate that csgD, which encodes a stationary phase-induced biofilm regulator, as well as ydaM, which encodes a diguanylate cyclase involved in activating csgD transcription, are novel negatively controlled RprA targets. As shown by extensive mutational analysis, direct binding of RprA to the 5'-untranslated and translational initiation regions of csgD mRNA inhibits translation and reduces csgD mRNA levels. In the case of ydaM mRNA, RprA base-pairs directly downstream of the translational start codon. In a feedforward loop, RprA can thus downregulate > 30 YdaM/CsgD-activated genes including those for adhesive curli fimbriae. However, during early stationary phase, when csgD transcription is strongly activated, the synthesis of csgD mRNA exceeds that of RprA, which allows the accumulation of CsgD protein. This situation is reversed when csgD transcription is shut off - for instance, later in stationary phase or during biofilm formation - or by conditions that further activate RprA expression via the Rcs two-component system. Thus, antagonistic regulation of csgD and RprA at the mRNA level integrates cell envelope stress signals with global gene expression during stationary phase and biofilm formation.

Zitieren

Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. / Mika, Franziska; Busse, Susan; Possling, Alexandra et al.
in: Molecular microbiology, Jahrgang 84, Nr. 1, 04.2012, S. 51-65.

Publikation: Beitrag in FachzeitschriftArtikelForschungPeer-Review

Mika F, Busse S, Possling A, Berkholz J, Tschowri N, Sommerfeldt N et al. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Molecular microbiology. 2012 Apr;84(1):51-65. doi: 10.1111/j.1365-2958.2012.08002.x
Mika, Franziska ; Busse, Susan ; Possling, Alexandra et al. / Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. in: Molecular microbiology. 2012 ; Jahrgang 84, Nr. 1. S. 51-65.
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abstract = "RprA is a small regulatory RNA known to weakly affect the translation of σ(S) (RpoS) in Escherichia coli. Here we demonstrate that csgD, which encodes a stationary phase-induced biofilm regulator, as well as ydaM, which encodes a diguanylate cyclase involved in activating csgD transcription, are novel negatively controlled RprA targets. As shown by extensive mutational analysis, direct binding of RprA to the 5'-untranslated and translational initiation regions of csgD mRNA inhibits translation and reduces csgD mRNA levels. In the case of ydaM mRNA, RprA base-pairs directly downstream of the translational start codon. In a feedforward loop, RprA can thus downregulate > 30 YdaM/CsgD-activated genes including those for adhesive curli fimbriae. However, during early stationary phase, when csgD transcription is strongly activated, the synthesis of csgD mRNA exceeds that of RprA, which allows the accumulation of CsgD protein. This situation is reversed when csgD transcription is shut off - for instance, later in stationary phase or during biofilm formation - or by conditions that further activate RprA expression via the Rcs two-component system. Thus, antagonistic regulation of csgD and RprA at the mRNA level integrates cell envelope stress signals with global gene expression during stationary phase and biofilm formation.",
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TY - JOUR

T1 - Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli

AU - Mika, Franziska

AU - Busse, Susan

AU - Possling, Alexandra

AU - Berkholz, Janine

AU - Tschowri, Natalia

AU - Sommerfeldt, Nicole

AU - Pruteanu, Mihaela

AU - Hengge, Regine

N1 - © 2012 Blackwell Publishing Ltd.

PY - 2012/4

Y1 - 2012/4

N2 - RprA is a small regulatory RNA known to weakly affect the translation of σ(S) (RpoS) in Escherichia coli. Here we demonstrate that csgD, which encodes a stationary phase-induced biofilm regulator, as well as ydaM, which encodes a diguanylate cyclase involved in activating csgD transcription, are novel negatively controlled RprA targets. As shown by extensive mutational analysis, direct binding of RprA to the 5'-untranslated and translational initiation regions of csgD mRNA inhibits translation and reduces csgD mRNA levels. In the case of ydaM mRNA, RprA base-pairs directly downstream of the translational start codon. In a feedforward loop, RprA can thus downregulate > 30 YdaM/CsgD-activated genes including those for adhesive curli fimbriae. However, during early stationary phase, when csgD transcription is strongly activated, the synthesis of csgD mRNA exceeds that of RprA, which allows the accumulation of CsgD protein. This situation is reversed when csgD transcription is shut off - for instance, later in stationary phase or during biofilm formation - or by conditions that further activate RprA expression via the Rcs two-component system. Thus, antagonistic regulation of csgD and RprA at the mRNA level integrates cell envelope stress signals with global gene expression during stationary phase and biofilm formation.

AB - RprA is a small regulatory RNA known to weakly affect the translation of σ(S) (RpoS) in Escherichia coli. Here we demonstrate that csgD, which encodes a stationary phase-induced biofilm regulator, as well as ydaM, which encodes a diguanylate cyclase involved in activating csgD transcription, are novel negatively controlled RprA targets. As shown by extensive mutational analysis, direct binding of RprA to the 5'-untranslated and translational initiation regions of csgD mRNA inhibits translation and reduces csgD mRNA levels. In the case of ydaM mRNA, RprA base-pairs directly downstream of the translational start codon. In a feedforward loop, RprA can thus downregulate > 30 YdaM/CsgD-activated genes including those for adhesive curli fimbriae. However, during early stationary phase, when csgD transcription is strongly activated, the synthesis of csgD mRNA exceeds that of RprA, which allows the accumulation of CsgD protein. This situation is reversed when csgD transcription is shut off - for instance, later in stationary phase or during biofilm formation - or by conditions that further activate RprA expression via the Rcs two-component system. Thus, antagonistic regulation of csgD and RprA at the mRNA level integrates cell envelope stress signals with global gene expression during stationary phase and biofilm formation.

KW - Bacterial Proteins/metabolism

KW - Binding Sites

KW - Biofilms/growth & development

KW - Cell Wall/metabolism

KW - Escherichia coli/genetics

KW - Escherichia coli Proteins/genetics

KW - Gene Expression Regulation, Bacterial

KW - Phosphorus-Oxygen Lyases/genetics

KW - Protein Biosynthesis

KW - RNA, Bacterial/genetics

KW - RNA, Messenger/biosynthesis

KW - Regulon

KW - Sigma Factor/metabolism

KW - Trans-Activators/genetics

U2 - 10.1111/j.1365-2958.2012.08002.x

DO - 10.1111/j.1365-2958.2012.08002.x

M3 - Article

C2 - 22356413

VL - 84

SP - 51

EP - 65

JO - Molecular microbiology

JF - Molecular microbiology

SN - 0950-382X

IS - 1

ER -

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