Chapter 27 : Dual-Function RNAs

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Bacteria have evolved elaborate responses to sense, protect against, and help recovery from stressful fluctuations in environmental conditions. In the past decade, small regulatory RNAs (sRNAs) have emerged as important players in the posttranscriptional regulation of various stress responses. Advances in deep sequencing have led to the identification of hundreds of these sRNAs, which range from 50 to 350 nucleotides (nt) in length, thereby greatly increasing the numbers of known sRNAs ( ). Usually, these sRNA regulators are thought to be noncoding and are generally presumed to act by modulating the stability and translation of mRNAs through short base-pairing interactions or by binding to and modulating the activities of RNA-binding proteins.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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Figure 1

Sugar-phosphate stress due to intracellular accumulation of phosphosugars triggers expression of the transcription factor SgrR. SgrR, in turn, induces transcription of the 227-nt sRNA SgrS, which also encodes a small, 43-aa protein, SgrT (blue). The other features of this sRNA include the base-pairing region (red) and the Hfq-binding region [poly(U) tail]. To relieve the sugar-phosphate stress, SgrS represses translation of mRNAs coding for sugar transporters (PtsG and ManXYZ) and other mRNAs involved in various metabolic pathways (Asd, AdiY, FolE, and PurR) to help restore metabolic homeostasis during stress conditions. SgrS also activates translation of a phosphatase (YigL) that dephosphorylates the phosphosugars for export out of the cell. SgrT, meanwhile, is expressed from SgrS later and inhibits the activity of the glucose transporter PtsG; thereby, both the sRNA and the encoded small protein act together in the same pathway to combat sugar-phosphate stress.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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Figure 2

RNAIII is part of the global regulatory locus known as the accessory gene regulator () locus, which encodes the components of an autoregulatory quorum-sensing system. The locus consists of two divergent transcripts, RNAII and RNAIII, which initiate from promoters P2 and P3, respectively. Increases in cell density lead to phosphorylation and activation of the DNA-binding response regulator AgrA. Phosphorylated AgrA in turn activates transcription from the P2 and P3 promoters, P3 activation leading to expression of RNAIII, the major effector molecule of the response. The secondary structure of the 514-nt RNAIII consists of 14 stem-loop structures with multiple base-pairing regions (red). RNAIII encodes a 26-aa δ-hemolysin protein (blue, ) but also acts as a posttranscriptional regulator of several mRNAs, most of which impact virulence. The RNA activates expression of Map, α-hemolysin, and MgrA proteins by either promoting a more open secondary structure surrounding the RBS by base-pairing in the case of and mRNAs or by stabilizing the RNA in the case of . RNAIII is also involved in translation inhibition and RNA degradation of various mRNAs involved in the early stages of infection.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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Figure 3

Psm-mec is located on staphylococcal cassette chromosome (SCC), next to the // genes, which confer methicillin resistance and its regulation. The 143- to 157-nt sRNA also encodes PSM-mec, a 22-aa cytolytic toxin with the ORF making up most of the transcript (blue). The protein plays a role in infection and immune evasion, while the sRNA represses the translation of mRNA by inhibiting translation and affecting the stability of the mRNA.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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Figure 4

The SR1 gene is encoded between and . Its transcription is repressed by CcpA and CcpN under glycolytic conditions. The 205-nt sRNA expressed under gluconeogenic conditions and in the presence of -arginine also encodes a small, 39-aa protein, SR1P (blue). The ORF and the base-pairing region overlap on this sRNA. In the presence of arginine, SR1 represses translation of the mRNA, the transcriptional activator of two arginine catabolic operons, and . The small protein SR1P plays a role in gluconeogenic conditions by binding to GapA and stabilizing the operon mRNA from degradation by an unknown mechanism. It also binds RNase J1 and enhances its activity. Thus, the activities of the small protein and base-pairing RNA affect different pathways.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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Figure 5

Pel/SagA sRNA is expressed from the pleiotropic effect locus of , comprising the operon. This 459-nt sRNA also encodes a 53-aa protein called streptolysin S (purple). Pel sRNA activates transcription of various mRNAs coding for different virulence factors, like Sic, Nga, and M protein, by an unknown mechanism. The sRNA also modulates maturation of cysteine protease SpeB.

Citation: Raina M, King A, Bianco C, Vanderpool C. 2019. Dual-Function RNAs, p 471-485. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0032-2018
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