Details
| Original language | English |
|---|---|
| Pages (from-to) | 51-65 |
| Number of pages | 15 |
| Journal | Molecular microbiology |
| Volume | 84 |
| Issue number | 1 |
| Publication status | Published - 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.
Keywords
- Bacterial Proteins/metabolism, Binding Sites, Biofilms/growth & development, Cell Wall/metabolism, Escherichia coli/genetics, Escherichia coli Proteins/genetics, Gene Expression Regulation, Bacterial, Phosphorus-Oxygen Lyases/genetics, Protein Biosynthesis, RNA, Bacterial/genetics, RNA, Messenger/biosynthesis, Regulon, Sigma Factor/metabolism, Trans-Activators/genetics
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In: Molecular microbiology, Vol. 84, No. 1, 04.2012, p. 51-65.
Research output: Contribution to journal › Article › Research › peer review
}
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 -