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Sponges and Predators in the Small RNA World

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  • Authors: Nara Figueroa-Bossi1, Lionello Bossi2
  • Editors: Gisela Storz3, Kai Papenfort4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University of Paris-Sud, University of Paris-Saclay, Gif-sur-Yvette, France; 2: Institute for Integrative Biology of the Cell (I2BC), CEA, CNRS, University of Paris-Sud, University of Paris-Saclay, Gif-sur-Yvette, France; 3: Division of Molecular and Cellular Biology, Eunice Kennedy Shriver National Institute of Child Health and Human Development, Bethesda, MD; 4: Department of Biology I, Microbiology, LMU Munich, Martinsried, Germany
  • Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0021-2018
  • Received 15 January 2018 Accepted 10 April 2018 Published 13 July 2018
  • Lionello Bossi, [email protected]
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  • Abstract:

    Most noncoding small RNAs (sRNAs) that regulate gene expression do so by base-pairing with mRNAs, affecting their translation and/or stability. Regulators as evolutionarily distant as the -encoded sRNAs of bacteria and the microRNAs (miRNAs) of higher eukaryotes share the property of targeting short sequence segments that occur in multiple copies in bacterial and eukaryotic transcriptomes. This target promiscuity has major implications for sRNA function. On the one hand, it allows the sRNA to coordinately control several different targets and thus be at the center of regulatory networks. On the other hand, it allows the existence of target mimics or decoys that divert the sRNA/miRNA away from bona fide targets and thus serve as mechanisms to regulate the regulator. In addition, by competing for pairing with the same sRNA, bona fide targets establish a cross talk that can impact on each other’s expression levels. Here we review evidence that target mimicry and competition are important components of the regulatory architecture of bacterial sRNA networks.

  • Citation: Figueroa-Bossi N, Bossi L. 2018. Sponges and Predators in the Small RNA World. Microbiol Spectrum 6(4):RWR-0021-2018. doi:10.1128/microbiolspec.RWR-0021-2018.

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/content/journal/microbiolspec/10.1128/microbiolspec.RWR-0021-2018
2018-07-13
2018-11-17

Abstract:

Most noncoding small RNAs (sRNAs) that regulate gene expression do so by base-pairing with mRNAs, affecting their translation and/or stability. Regulators as evolutionarily distant as the -encoded sRNAs of bacteria and the microRNAs (miRNAs) of higher eukaryotes share the property of targeting short sequence segments that occur in multiple copies in bacterial and eukaryotic transcriptomes. This target promiscuity has major implications for sRNA function. On the one hand, it allows the sRNA to coordinately control several different targets and thus be at the center of regulatory networks. On the other hand, it allows the existence of target mimics or decoys that divert the sRNA/miRNA away from bona fide targets and thus serve as mechanisms to regulate the regulator. In addition, by competing for pairing with the same sRNA, bona fide targets establish a cross talk that can impact on each other’s expression levels. Here we review evidence that target mimicry and competition are important components of the regulatory architecture of bacterial sRNA networks.

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Figures

Image of FIGURE 1
FIGURE 1

Regulation of chitosugar uptake in and . The gene and the operon encode proteins involved in the uptake and utilization of chitin-derived sugars. When no chitosugars are available, ChiP synthesis is prevented by constitutively made ChiX sRNA, which represses translation of mRNA (made at a relatively high basal level), while the operon is repressed transcriptionally by the NagC repressor (not shown). ChiX further lowers the uninduced levels of the mRNA by pairing with a sequence in the intercistronic region. In the presence of chitosugars, transcriptional activation of operon produces a large accumulation of the polycistronic mRNA. Now in excess over ChiX, this mRNA titrates out ChiX through base-pairing and promotes its degradation. ChiX depletion results in the derepression of the mRNA.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0021-2018
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Image of FIGURE 2
FIGURE 2

sRNA sponging by a tRNA spacer sequence. The sRNAs RybB (blue) and RyhB (purple) are made in response to envelope stress or iron limitation, respectively. An ∼50-nt RNA, named 3′ETS (red), released by RNase E cleavage of the tRNA precursor (top) can form stable base-pair interactions with both RybB and RyhB. This allows 3′ETS to capture and sequester RybB and RyhB molecules that are made adventitiously (in the absence of any stress) due to transcriptional noise (left). Under inducing conditions (envelope stress or iron limitation), accumulation of either RybB or RyhB saturates the sponging capacity of 3′ETS. This sets the threshold concentration (dotted line) that either of the two sRNAs must attain to begin performing its regulatory task: downregulation of OMPs for RybB (middle) or of nonessential iron-binding proteins for RyhB (right).

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0021-2018
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Image of FIGURE 3
FIGURE 3

Target-mediated derepression of the GcvB regulon. The sRNA GcvB downregulates several mRNAs encoding amino acid and small peptide transporters. Among these is the mRNA (left). Presence of a leaky Rho-independent transcription terminator in the spacer between and causes a fraction of transcripts initiating at the promoter to terminate prematurely in the spacer region (right). RNase E cleavage of the prematurely terminated transcripts generates SroC, an ∼150-nt RNA, which captures GcvB through a base-pairing interaction and destabilizes it. As a result, all of the GcvB targets become derepressed. Since the SroC precursor RNA itself is one of these targets, SroC activity drives a feedforward regulatory loop.

Source: microbiolspec July 2018 vol. 6 no. 4 doi:10.1128/microbiolspec.RWR-0021-2018
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Image of FIGURE 4
FIGURE 4

A sponging relay model. Depicted are two hypothetical sRNA networks (A and B) linked by an mRNA node (cyan-filled circle). (Top) The two sRNAs downregulate their respective targets. (Bottom) A transcriptional regulatory event leads to a large increase in the concentration of one of the mRNAs in network A (yellow-filled circle). The accumulated mRNA sequesters and destabilizes its cognate sRNA, resulting in the derepression of the entire network A, including the nodal mRNA. In turn, the latter acts as a sponge for cognate sRNA in network B, thus relieving, or attenuating (depicted here), the repression of the B network.

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