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Riboregulation of bacterial and archaeal transposition

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The coexistence of transposons with their hosts depends largely on transposition levels being tightly regulated to limit the mutagenic burden associated with frequent transposition. For ‘DNA‐based’ (class II) bacterial transposons there is growing evidence that regulation through small noncoding RNAs and/or the RNA‐binding protein Hfq are prominent mechanisms of defense against transposition. Recent transcriptomics analyses have identified many new cases of antisense RNAs (asRNA) that potentially could regulate the expression of transposon‐encoded genes giving the impression that asRNA regulation of DNA‐based transposons is much more frequent than previously thought. Hfq is a highly conserved bacterial protein that plays a central role in posttranscriptional gene regulation and stress response pathways in many bacteria. Three different mechanisms for Hfq‐directed control of bacterial transposons have been identified to date highlighting the versatility of this protein as a regulator of bacterial transposons. There is also evidence emerging that some DNA‐based transposons encode RNAs that could regulate expression of host genes. In the case of IS200, which appears to have lost its ability to transpose, contributing a regulatory RNA to its host could account for the persistence of this mobile element in a wide range of bacterial species. It remains to be seen how prevalent these transposon‐encoded RNA regulators are, but given the relatively large amount of intragenic transcription in bacterial genomes, it would not be surprising if new examples are forthcoming. WIREs RNA 2016, 7:382–398. doi: 10.1002/wrna.1341 This article is categorized under: RNA Interactions with Proteins and Other Molecules > Protein–RNA Interactions: Functional Implications Translation > Translation Regulation Regulatory RNAs/RNAi/Riboswitches > Regulatory RNAs
Mechanisms of antisense control of transposase expression. (a) Base‐pairing between the IS10 asRNA (RNA‐OUT) and transposase mRNA (RNA‐IN) initiates between the terminal loop of RNA‐OUT and the single‐stranded 5′ end of RNA‐IN and propagates to form a 35‐bp duplex. Pairing sequesters the Shine‐Dalgarno (SD) sequence and start codon (AUG) of RNA‐IN such that the 30S ribosome is unable to bind and initiate translation. A secondary effect of pairing is the recruitment of RNase III, which leads to the degradation of RNA‐IN. (b) The IS30 asRNA (RNA‐C) is complementary to 150‐nt of the transposase (ORF‐A) coding region. RNA‐C inhibits translation of ORF‐A, likely by interfering with transiting ribosomes. (c) Like IS10, the IS200 asRNA (art200) is complementary to the translation initiation region of the transposase (tnpA). Intermolecular pairing initiates with a 3‐nt kissing‐loop interaction that propagates approximately halfway through the stem‐loop structure of each RNA. Base‐pairing extends over ~40‐nt in the final paired species and includes a putative translational enhancer sequence. Pairing prevents 30S ribosome binding and results in degradation of art200 and most likely tnpA.
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Regulation of host gene expression by transposon associated sRNAs. (a) Genome context of ORF1182, ORF1183, and one copy of RNA‐257 in S. solfataricus. In media containing low phosphate, RNA‐257 is poorly expressed and accordingly the 1183 mRNA (coding sequence, blue; 3′UTR, black) is stable and presumably translated. RNA‐257 is induced in the presence of high phosphate and subsequently base‐pairs with the distal coding region and 3′UTR of 1183. This pairing interaction results in active degradation of the 1183 transcript. Potentially, the 3′UTR of ISC1904 transposase mRNA (ORF1182) could pair with the ORF1183 transcript and direct the degradation of the latter (not shown). (b) Generalized schematic of the IS1341 transposase (10 copies) and the associated sense‐overlapping transcripts (sotRNAs; only 5 shown) in H. salinarum. The sotRNAs are heterogenous in size and exact location relative to the tnpB coding sequence, but all 10 are encoded at the 3′ end (~150‐nt upstream of the stop codon to ~75‐nt into the 3′UTR). As cells progress to stationary phase, tnpB levels decrease while sotRNA levels increase. In contrast, overexpression of the TfbD transcription factor represses sotRNA expression while increasing tnpB levels. Potential targets of IS1341 sotRNAs have not been defined but VNG_sot0042 does impact on growth rate. (c) Expression of the IS200 asRNA (art200) is increased in response to growth phase and conditions simulating infection of mammalian hosts. Art200 (blue wavy lines) appears to affect the expression of host genes in Salmonella.
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Mechanisms of Hfq‐mediated repression of transposase expression. (a) Model for Hfq catalysis of IS10 antisense pairing. Nucleotides in RNA‐IN and RNA‐OUT involved in pairing are partially sequestered in secondary structure (i) which could limit the rate of intermolecular base‐pairing. Hfq (green circles) binding to both RNAs alters secondary structure (ii) in a manner that exposes the pairing sequences in each RNA and accordingly accelerates the rate of pairing. (b) Hfq competes with the 30S ribosome for binding to transposase mRNA. In the IS10 system (i), the distal surface of Hfq binds to a sequence in the 5′UTR overlapping the SD. This interaction is sufficient for blocking 30S ribosome binding. In contrast, Hfq binds a region 5′ to the IS200 tnpA (ii) that likely acts as a translational enhancer. This interaction is also able to block 30S binding to tnpA. (c) Transcriptional regulation of IS50 transposase by Hfq. Hfq and CRP are negative regulators of IS50 transposase transcription. As Hfq positively regulates CRP, it is likely that the Hfq effect is indirect and exerted solely through regulation of CRP levels. It is not known if CRP directly affects IS50 transcription or acts through an intermediary (indicated by ‘?’).
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