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Small RNAs in Bacterial Virulence and Communication

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  • Authors: Sarah L. Svensson1, Cynthia M. Sharma2
  • Editors: Indira T. Kudva3, Paul J. Plummer4
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Research Center for Infectious Diseases (ZINF), University of Würzburg, Josef-Schneider-Straße 2 / Bau D15, 97080 Würzburg, Germany; 2: Research Center for Infectious Diseases (ZINF), University of Würzburg, Josef-Schneider-Straße 2 / Bau D15, 97080 Würzburg, Germany; 3: National Animal Disease Center, Agricultural Research Service, U.S. Department of Agriculture, Ames, IA; 4: Department of Veterinary Diagnostic and Production Animal Medicine, College of Veterinary Medicine, Iowa State University, Ames, IA
  • Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
  • Received 17 September 2015 Accepted 14 January 2016 Published 06 May 2016
  • Cynthia M. Sharma, cynthia.sharma@uni-wuerzburg.de
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  • Abstract:

    Bacterial pathogens must endure or adapt to different environments and stresses during transmission and infection. Posttranscriptional gene expression control by regulatory RNAs, such as small RNAs and riboswitches, is now considered central to adaptation in many bacteria, including pathogens. The study of RNA-based regulation (riboregulation) in pathogenic species has provided novel insight into how these bacteria regulate virulence gene expression. It has also uncovered diverse mechanisms by which bacterial small RNAs, in general, globally control gene expression. Riboregulators as well as their targets may also prove to be alternative targets or provide new strategies for antimicrobials. In this article, we present an overview of the general mechanisms that bacteria use to regulate with RNA, focusing on examples from pathogens. In addition, we also briefly review how deep sequencing approaches have aided in opening new perspectives in small RNA identification and the study of their functions. Finally, we discuss examples of riboregulators in two model pathogens that control virulence factor expression or survival-associated phenotypes, such as stress tolerance, biofilm formation, or cell-cell communication, to illustrate how riboregulation factors into regulatory networks in bacterial pathogens.

  • Citation: Svensson S, Sharma C. 2016. Small RNAs in Bacterial Virulence and Communication. Microbiol Spectrum 4(3):VMBF-0028-2015. doi:10.1128/microbiolspec.VMBF-0028-2015.

Key Concept Ranking

Mobile Genetic Elements
0.87911665
Infection and Immunity
0.80086416
Gene Expression and Regulation
0.7692271
PhoPQ Two-Component Regulatory System
0.45508993
Type III Secretion System
0.41661718
Type VI Secretion System
0.41661718
0.87911665

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/content/journal/microbiolspec/10.1128/microbiolspec.VMBF-0028-2015
2016-05-06
2017-09-19

Abstract:

Bacterial pathogens must endure or adapt to different environments and stresses during transmission and infection. Posttranscriptional gene expression control by regulatory RNAs, such as small RNAs and riboswitches, is now considered central to adaptation in many bacteria, including pathogens. The study of RNA-based regulation (riboregulation) in pathogenic species has provided novel insight into how these bacteria regulate virulence gene expression. It has also uncovered diverse mechanisms by which bacterial small RNAs, in general, globally control gene expression. Riboregulators as well as their targets may also prove to be alternative targets or provide new strategies for antimicrobials. In this article, we present an overview of the general mechanisms that bacteria use to regulate with RNA, focusing on examples from pathogens. In addition, we also briefly review how deep sequencing approaches have aided in opening new perspectives in small RNA identification and the study of their functions. Finally, we discuss examples of riboregulators in two model pathogens that control virulence factor expression or survival-associated phenotypes, such as stress tolerance, biofilm formation, or cell-cell communication, to illustrate how riboregulation factors into regulatory networks in bacterial pathogens.

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Figures

Image of FIGURE 1
FIGURE 1

Genomic location and regulatory relationships between bacterial riboregulators and their mRNA targets. Riboregulators are depicted in red; target mRNAs are shown in blue. Flanking open reading frames (ORFs) are shown in black. Arrows indicate transcriptional start sites. -encoded antisense RNAs are transcribed from the opposite strand to their target mRNAs and can overlap with target 5′/3′ untranslated regions (UTRs) (top panel) and/or the mRNA ORF (bottom panel). -encoded sRNAs can be expressed from distinct regions of the chromosome from their target genes: either from stand-alone genes encoded intergenically (top panel) or from ORFs/3′UTRs via either processing or internal transcriptional start sites (bottom panel). Extended UTR elements of adjacent operons can allow for coregulation of related genes at the posttranscriptional level. The long-antisense RNA (lasRNA) of the excludon paradigm arises from transcription of an extended 5′UTR that has complementarity to a divergently transcribed operon (top panel). Also, extended 3′UTR elements can potentially base-pair with transcripts expressed from convergently transcribed operons (bottom panel). -elements within mRNAs themselves can regulate expression of their associated transcripts. These include ligand-binding riboswitches (top panel) and temperature-responsive RNA thermosensors (bottom panel).

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
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FIGURE 2

Mechanisms of posttranscriptional control by regulatory RNAs. Gene repression (left) and activation (right) mechanisms used by base-pairing sRNAs (depicted in red) for direct regulation of target mRNAs (shown in blue) at the level of translation or stability. Base-pairing interaction sites in mRNAs and sRNAs are shown with blue- and red-lined boxes, respectively. Potential RNase cleavage sites are indicated with an orange asterisk. Also participating are ribosomes and RNases. TIR, translation initiation region including RBS and start codon. Potential sRNA interaction sites in regulated target mRNAs, starting from the TSS (transcriptional start site) to the transcriptional terminator (TERM). Targeting/titration of other regulatory molecules by riboregulators acting as so-called sponges to affect gene expression. RNA sponges can be stand-alone sRNAs, regions of mRNAs themselves (either intact or processed), or those derived from housekeeping RNAs such as the 3′ external transcribed spacer (3′ ETS) of tRNAs. They can target either sRNA or protein regulators and have been shown to sequester them away from their targets, trigger their degradation, and/or modulate their regulatory activity.

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
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FIGURE 3a

Numerous riboregulators participate in quorum sensing and virulence regulation of . Riboregulation of the ToxT virulence regulon in response to temperature. The central transcriptional regulator ToxT (blue circles, center) activates virulence and colonization factor genes, such as (toxin-coregulated pilus), (cholera toxin), and (accessory colonization factor). ToxT also autoregulates its own transcription. Levels of ToxT are also modulated in response to temperature by a FourU RNA thermometer, with increased translation at the 37°C host temperature. ToxT also activates the sRNAs TarB, which represses translation of the ORF of mRNA, and TarA, which represses mRNA (glucose uptake). The VrrA sRNA also represses .

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
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FIGURE 3b

Numerous riboregulators participate in quorum sensing and virulence regulation of . The Qrr sRNAs mediate the switch between low and high cell-density physiologies via reciprocal posttranscriptional regulation of the master regulators AphA and HapR. autoinducers (AI-2 and CAI-1) are made by LuxS and CqsA, respectively, and accumulate extracellularly. Phosphorelay systems headed by LuxPQ or CqsS (AI-2 and CAI-1, respectively) detect autoinducers. Left panel: Low bacterial density. Continued phosphorylation of LuxO at low autoinducer conditions leads to transcription of the Qrr sRNAs, which act along with the RNA chaperone Hfq to activate translation of mRNA. In turn, AphA expression induces the ToxT virulence regulon (see panel ), as well as genes required for biofilm formation (). The Qrrs also repress the mRNA, which encodes the high-density master regulator (see right panel). Right panel: High bacterial density. High autoinducer concentration reduces levels of phosphorylated LuxO and, thus, Qrr expression. The mRNA is no longer destabilized, allowing translation of the HapR regulator. HapR activates genes that mediate biofilm dispersal and competence. In addition, genes activated by AphA at low density, such as , as well as itself and its regulated genes, are repressed by HapR. Genes encoding the type VI secretion system are also induced. Finally, feedback regulation occurs via HapR activation of Qrr expression and Qrr repression of the mRNA. The sRNA VqmR is activated by the transcriptional regulator VqmA and posttranscriptionally represses mRNA and mRNA, encoding the RTX toxin, as well as six other mRNAs.

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
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FIGURE 4

The dual-function sRNA RNAIII of reciprocally regulates expression of secreted virulence factors and surface proteins in response to cell density. (A) Genomic context and transcriptional regulation of the quorum sensing locus, including the dual-function RNAIII. The RNAII mRNA (black) encodes proteins required for synthesis and detection of the peptide pheromone (, green and red open reading frames [ORFs]). Under high cell density and high autoinducer concentration, phosphorylated AgrA (red) activates transcription of the RNAIII sRNA (blue). RNAIII encodes δ-haemolysin ( ORF) and is the major mediator of Agr regulation. (B) Overall integration of RNAIII posttranscriptional activities promotes toxin expression and represses expression of secreted proteins. Center: General structure of RNAIII with the coding region (light blue) and C-rich loops (red). The RNAIII molecule directly activates the mRNA encoding α-haemolysin (). Also, together with the double-strand-specific RNase III, the sRNA directly represses numerous genes encoding surface-associated proteins (, , SA2353, SA1000). RNAIII also represses translation of Rot, a repressor of toxin gene expression.

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015
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Tables

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TABLE 1

Examples of PAI-encoded sRNAs and of riboregulators of bacterial virulence/colonization factors

Source: microbiolspec May 2016 vol. 4 no. 3 doi:10.1128/microbiolspec.VMBF-0028-2015

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