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Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress.

ABSTRACT: The Escherichia coli small RNA SgrS controls a metabolic stress response that occurs upon accumulation of certain glycolytic intermediates. SgrS base pairs with and represses translation of ptsG and manXYZ mRNAs, which encode sugar transporters, and activates translation of yigL mRNA, encoding a sugar phosphatase. This study defines four new genes as direct targets of E. coli?SgrS. These new targets, asd, adiY, folE and purR, encode transcription factors or enzymes of diverse metabolic pathways, including aspartate semialdehyde dehydrogenase, arginine decarboxylase gene activator, GTP cyclohydrolase I and a repressor of purine biosynthesis, respectively. SgrS represses translation of each of the four target mRNAs via distinct mechanisms. SgrS binding sites overlapping the Shine-Dalgarno sequences of adiY and folE mRNAs suggest that SgrS pairing with these targets directly occludes ribosome binding and prevents translation initiation. SgrS binding within the purR coding sequence recruits the RNA chaperone Hfq to directly repress purR translation. Two separate SgrS binding sites were found on asd mRNA, and both are required for full translational repression. Ectopic overexpression of asd, adiY and folE is specifically detrimental to cells experiencing glucose-phosphate stress, suggesting that SgrS-dependent repression of the metabolic functions encoded by these targets promotes recovery from glucose-phosphate stress.

SUBMITTER: Bobrovskyy M

PROVIDER: S-EPMC4996119 | biostudies-literature | 2016 Jan

REPOSITORIES: biostudies-literature

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Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress.

Bobrovskyy Maksym M Vanderpool Carin K CK

Molecular microbiology 20151026 2

The Escherichia coli small RNA SgrS controls a metabolic stress response that occurs upon accumulation of certain glycolytic intermediates. SgrS base pairs with and represses translation of ptsG and manXYZ mRNAs, which encode sugar transporters, and activates translation of yigL mRNA, encoding a sugar phosphatase. This study defines four new genes as direct targets of E. coli SgrS. These new targets, asd, adiY, folE and purR, encode transcription factors or enzymes of diverse metabolic pathways, ...[more]

PMID: 26411266

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Project description:Pseudomonas aeruginosa is one of the most critical opportunistic pathogens in humans, able to cause both lethal acute and chronic lung infections. In previous work, we indicated that the small RNA ErsA plays a role in the regulatory network of P. aeruginosa pathogenicity in airways infection. To give further insight into the lifestyle functions that could be either directly or indirectly regulated by ErsA during infection, we reanalyzed the categories of genes whose transcription appeared dysregulated in an ersA knock-out mutant of the P. aeruginosa PAO1 reference strain. This preliminary analysis indicated ErsA as a candidate co-modulator of denitrification and in general, the anaerobiosis response, a characteristic physiologic state of P. aeruginosa during chronic infection of the lung of cystic fibrosis (CF) patients. To explain the pattern of dysregulation of the anaerobic-lifestyle genes in the lack of ErsA, we postulated that ErsA regulation could target the expression of Anr, a well-known transcription factor that modulates a broad regulon of anoxia-responsive genes, and also Dnr, required for the transcription activation of the denitrification machinery. Our results show that ErsA positively regulates Anr expression at the post-transcriptional level while no direct ErsA-mediated regulatory effect on Dnr was observed. However, Dnr is transcriptionally downregulated in the absence of ErsA and this is consistent with the well-characterized regulatory link between Anr and Dnr. Anr regulatory function is critical for P. aeruginosa anaerobic growth, both through denitrification and fermentation of arginine. Interestingly, we found that, differently from the laboratory strain PAO1, ErsA deletion strongly impairs the anaerobic growth by both denitrification and arginine fermentation of the RP73 clinical isolate, a multi-drug resistant P. aeruginosa CF-adapted strain. This suggests that P. aeruginosa adaptation to CF lung might result in a higher dependence on ErsA for the transduction of the multiple signals to the regulatory network of key functions for survivance in such a complex environment. Together, our results suggest that ErsA takes an upper place in the regulatory network of airways infection, transducing host inputs to biofilm-related factors, as underlined in our previous reports, and to functions that allow P. aeruginosa to thrive in low-oxygen conditions.

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Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress.

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Diverse mechanisms of post-transcriptional repression by the small RNA regulator of glucose-phosphate stress.

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