Stress sigma factor RpoS degradation and translation are sensitive to the state of central metabolism

Battesti, Aurélia; Majdalani, Nadim; Gottesman, Susan

doi:10.1073/pnas.1504639112

Cited by 65 publications

(58 citation statements)

References 35 publications

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“…A22 inhibits the actinlike MreB protein and provides superior activation of the Rcs phosphorelay compared with bile salts (Fig. S4B) (45,50). As expected from our previous results ( induction and did not up-regulate RicI (Fig.…”

Section: Resultssupporting

confidence: 83%

“…S4D). These differences in protein levels might depend on specific proteolytic factors targeting the σ S protein (50). Interestingly, we found that σ S degradation also preceded inhibition of RprA expression: expression levels of full-length RprA and processed RprA reached the prestress status ∼15 min after cells were reinoculated in fresh media.…”

Section: Resultsmentioning

confidence: 75%

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Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Papenfort

Espinosa

Casadesús

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Horizontal gene transfer via plasmid conjugation is a major driving force in microbial evolution but constitutes a complex process that requires synchronization with the physiological state of the host bacteria. Although several host transcription factors are known to regulate plasmid-borne transfer genes, RNA-based regulatory circuits for host-plasmid communication remain unknown. We describe a posttranscriptional mechanism whereby the Hfq-dependent small RNA, RprA, inhibits transfer of pSLT, the virulence plasmid of Salmonella enterica. RprA employs two separate seed-pairing domains to activate the mRNAs of both the sigma-factor σ S and the RicI protein, a previously uncharacterized membrane protein here shown to inhibit conjugation. Transcription of ricI requires σ S and, together, RprA and σ S orchestrate a coherent feedforward loop with AND-gate logic to tightly control the activation of RicI synthesis. RicI interacts with the conjugation apparatus protein TraV and limits plasmid transfer under membrane-damaging conditions. To our knowledge, this study reports the first small RNA-controlled feedforward loop relying on posttranscriptional activation of two independent targets and an unexpected role of the conserved RprA small RNA in controlling extrachromosomal DNA transfer.RprA | sRNA | feedforward control | plasmid conjugation | Hfq

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Section: Resultssupporting

confidence: 83%

Section: Resultsmentioning

confidence: 75%

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Papenfort

Espinosa

Casadesús

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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“…These stressresponse genes are direct targets of ppGpp-regulated transcription and are responsible for the expression of rRNAs and tRNAs and RpoS accumulation, respectively (26,27). Expression of iraP has been shown to increase in response to increased ppGpp levels, whereas expression from the rrsB P1 promoter decreases during the stringent response (27)(28)(29). When normalized to Fig.…”

Section: Phers Editing Is Required For Proper Regulation Of Phenylalamentioning

confidence: 99%

Translation quality control is critical for bacterial responses to amino acid stress

Bullwinkle

Ibba

2016

Proc. Natl. Acad. Sci. U.S.A.

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Gene expression relies on quality control for accurate transmission of genetic information. One mechanism that prevents amino acid misincorporation errors during translation is editing of misacylated tRNAs by aminoacyl-tRNA synthetases. In the absence of editing, growth is limited upon exposure to excess noncognate amino acid substrates and other stresses, but whether these physiological effects result solely from mistranslation remains unclear. To explore if translation quality control influences cellular processes other than protein synthesis, an Escherichia coli strain defective in Tyr-tRNA Phe editing was used. In the absence of editing, cellular levels of aminoacylated tRNA Phe were elevated during amino acid stress, whereas in the wild-type strain these levels declined under the same growth conditions. In the editing-defective strain, increased levels of aminoacylated tRNA Phe led to continued synthesis of the PheL leader peptide and attenuation of pheA transcription under amino acid stress. Consequently, in the absence of editing, activation of the phenylalanine biosynthetic operon becomes less responsive to phenylalanine limitation. In addition to raising aminoacylated tRNA levels, the absence of editing lowered the amount of deacylated tRNA Phe in the cell. This reduction in deacylated tRNA was accompanied by decreased synthesis of the second messenger guanosine tetraphosphate and limited induction of stringent response-dependent gene expression in editing-defective cells during amino acid stress. These data show that a single qualitycontrol mechanism, the editing of misacylated aminoacyl-tRNAs, provides a critical checkpoint both for maintaining the accuracy of translation and for determining the sensitivity of transcriptional responses to amino acid stress.translation | quality control | stress | stringent response

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“…The presence of rare codons within the rpoS ORF also positively contributes to mRNA stability by decreasing degradation by RNaseE (Kolmsee and Hengge 2011). Additionally, AceE, a subunit of pyruvate dehydrogenase, also influences rpoS ORF translation via an undefined mechanism (Battesti et al 2015). Finally, the MiaA tRNA modification enzyme is required for efficient translation of the rpoS ORF translation (Thompson and Gottesman 2014).…”

Section: Introductionmentioning

confidence: 99%

The i⁶A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation

Aubee

Olu

Thompson

2016

RNA

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The translation of rpoS (σ S ), the general stress/stationary phase sigma factor, is tightly regulated at the post-transcriptional level by several factors via mechanisms that are not clearly defined. One of these factors is MiaA, the enzyme necessary for the first step in the N 6 -isopentyl-2-thiomethyladenosinemethyladenosine 37 (ms 2 i 6 A37) tRNA modification. We tested the hypothesis that an elevated UUX-Leucine/total leucine codon ratio can be used to identify transcripts whose translation would be sensitive to loss of the MiaA-dependent modification. We identified iraP as another candidate MiaA-sensitive gene, based on the UUX-Leucine/ total leucine codon ratio. An iraP-lacZ fusion was significantly decreased in the absence of MiaA, consistent with our predictive model. To determine the role of MiaA in UUX-Leucine decoding in rpoS and iraP, we measured β-galactosidasespecific activity of miaA − rpoS and iraP translational fusions upon overexpression of leucine tRNAs. We observed suppression of the MiaA effect on rpoS, and not iraP, via overexpression of tRNA LeuX but not tRNA LeuZ . We also tested the hypothesis that the MiaA requirement for rpoS and iraP translation is due to decoding of UUX-Leucine codons within the rpoS and iraP transcripts, respectively. We observed a partial suppression of the MiaA requirement for rpoS and iraP translational fusions containing one or both UUX-Leucine codons removed. Taken together, this suggests that MiaA is necessary for rpoS and iraP translation through proper decoding of UUX-Leucine codons and that rpoS and iraP mRNAs are both modification tunable transcripts (MoTTs) via the presence of the modification.

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Stress sigma factor RpoS degradation and translation are sensitive to the state of central metabolism

Cited by 65 publications

References 35 publications

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Translation quality control is critical for bacterial responses to amino acid stress

The i⁶A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation

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Stress sigma factor RpoS degradation and translation are sensitive to the state of central metabolism

Cited by 65 publications

References 35 publications

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella

Translation quality control is critical for bacterial responses to amino acid stress

The i6A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation

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The i⁶A37 tRNA modification is essential for proper decoding of UUX-Leucine codons during rpoS and iraP translation