Chapter 17 : Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation

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Bacteria use the production, release, and detection of extracellular chemical signaling molecules called autoinducers (AIs) to regulate gene expression at the population level, a widespread phenomenon known as quorum sensing (QS). The first reviews of small RNA (sRNA) control of QS were published in 2006 and 2007 ( ). At that time, two QS systems had been described that are entirely dependent on sRNA-based regulation, namely, the QS circuits of the Gram-negative family and the QS circuit of the Gram-positive staphylococci. A decade later, these two examples have become paradigms of sRNA-based regulation, and have taught us important regulatory principles relevant not only to QS but to bacterial sRNA-based regulation in general. I begin this review by describing the progress made in understanding sRNA-based execution of the QS response in these two systems. In many other bacteria the core executors of QS are not sRNAs, but sRNAs are nevertheless identified as auxiliary regulators that directly or indirectly affect components of the QS machinery. In particular, sRNA-based regulation of the production of enzymes that catalyze AI synthesis appears as a common trend across numerous unrelated QS circuits, and such examples will be highlighted. Due to space limitations, this review is solely focused on riboregulation carried out by small -acting RNA molecules that are encoded at loci distinct from those of their target(s), thereby excluding -acting regulatory RNA elements such as riboswitches and attenuators, as well as antisense RNA transcripts. Notably, QS has only been sparsely connected to -acting riboregulation in the literature thus far ( ).

Citation: Svenningsen S. 2019. Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation, p 283-304. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0017-2018
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Figure 1

RNAIII of . (a) The QS pathway of . Direct posttranscriptional effects of RNAIII (blue oval) on target mRNAs are shown as green arrows (positive regulation) or red blocked arrows (negative regulation). The positive feedback loop of the system is depicted as light blue arrows from the RNAII operon to AgrA∼P. Transcriptional regulation is shown by black arrows. Groups of genes that are regulated but in an RNAIII-independent manner are included as targets of AgrA∼P, although direct transcriptional regulation by AgrA∼P has only been demonstrated for RNAII, RNAIII, and the α- and β-PSMs ( ). (b) Secondary structure of RNAIII. The ORF is shown in black. Three C-rich regions involved in base-pairing with target mRNAs are shown in red. Adapted from structure determined by Benito et al. ( ) and depicted using Forna ( ). (c) The RNA-based double selector switch of .

Citation: Svenningsen S. 2019. Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation, p 283-304. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0017-2018
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Figure 2

QS regulation by the Qrr sRNAs in . (a) Secondary structure of Qrr4. The region that is completely conserved among Qrr1 to -5 in is shown in red. The 9 nt of stem-loop 1 that are missing in Qrr1 are shown in green. Modified from Shao et al. ( ) and depicted using Forna ( ). (b) The QS pathway of . The symbols and colors are used as in Fig. 1 . Direct autorepression by the transcription factors is omitted for clarity but has been demonstrated for all three of the transcription factors shown (LuxO, AphA, and LuxR). LCD genes, genes expressed at low cell density; HCD genes, genes expressed at high cell density.

Citation: Svenningsen S. 2019. Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation, p 283-304. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0017-2018
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Figure 3

sRNA-based regulation of AI synthase production. AI synthases are shown as red rectangles with a red arrow pointing to the structure of the AI(s) they produce. A curved arrow from the AI to its receptor (brown rectangles) indicates activation of the receptor upon binding to the AI, whereas a curved blocked arrow indicates inactivation of the receptor upon AI binding. Posttranscriptional regulatory interactions are shown by green arrows (increased translation) or red blocked arrows (decreased translation), and transcriptional regulatory interactions are depicted in black. Known signals/conditions that affect sRNA expression are shown below each sRNA. (a) Positive feedback control of 3-oxo-C6-HSL synthesis in . (b) Repression of the HAI-1 synthase, LuxM, by the Qrr sRNAs in . Blocked arrow from HAI-1 to LuxN indicates that HAI-1 binding blocks the kinase activity of LuxN. The phosphatase activity of LuxN is not affected by AI binding ( ). The dashed arrow indicates that LuxN promotes transcription indirectly through a phosphorelay when LuxN is acting as a kinase (see Fig. 2b ). (c) Positive feedback control of C8-HSL synthesis in involves a single Qrr sRNA. Symbols are as in panel b. (d) Positive effect of the RsmYZ sRNAs on the LasI and RhlI AHL synthases of . Regulatory interactions between the two QS systems are excluded for clarity. (e) Positive effects of the ReaL and PhrS sRNAs on PQS production in . (f) Repression of AHL production by the RscR1 sRNA. SinI produces a range of long-chain AHLs, exemplified here by -(tetrahydro-2-oxo-3-furanyl)-dodecanamide ( ). (g) CyaR sRNA represses translation of the AI-2 synthase LuxS in . The depicted isoform of AI-2 is -2-methyl-2,3,3,4-tetrahydroxytetrahydrofuran (R-THMF), which is the AI-2 isoform typically recognized by the Lsr machinery that transports AI-2 into the cytoplasm. AI-2 is phosphorylated before AI-2∼P binds and inactivates the LsrR transcriptional repressor. Inactivation of LsrR feeds back to affect extra- and intracellular AI-2 levels because it derepresses production of the Lsr transport system, which leads to increased AI-2 internalization and depletion of extracellular AI-2. That feedback loop is not included here since it does not affect AI-2 synthesis (reviewed in reference ).

Citation: Svenningsen S. 2019. Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation, p 283-304. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0017-2018
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Figure 4

Posttranscriptional control of key biofilm regulators in K-12. Direct posttranscriptional effects of sRNAs (blue ovals) on five protein regulators central to the biofilm/motility switch (colored rectangles) are shown as green arrows (positive regulation) or red blocked arrows (negative regulation). Only direct sRNA-target interactions are shown, although several additional sRNAs indirectly regulate one or more of the five targets ( ). Some transcriptional regulation is included to provide context, but many important regulators and interactions are omitted for clarity. These include all proteins involved in c-di-GMP signaling, and interactions concerning σ-factor competition (reviewed in reference ).

Citation: Svenningsen S. 2019. Small RNA-Based Regulation of Bacterial Quorum Sensing and Biofilm Formation, p 283-304. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0017-2018
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