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Chapter 18 : Regulatory RNAs in Virulence and Host-Microbe Interactions

Author: Alexander J. Westermann1
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Affiliations: 1: Institute of Molecular Infection Biology, University of Würzburg; 2: Helmholtz Institute for RNA-Based Infection Research, D-97080 Würzburg, Germany
Content Type: Monograph
Publication Year: 2019

Category: Microbial Genetics and Molecular Biology

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Abstract:

Infectious diseases caused by bacterial pathogens still constitute one of the major human health threats ( ). Within the host body, pathogenic bacteria face a wide variety of hostile microenvironments and encounter numerous different host cell types as well as commensal bacteria of the resident microbiota. To cope with these environmental changes and respond adequately to any interacting cell, bacterial pathogens have to tightly control their gene expression during infection, in part by means of regulatory RNAs.

Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
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Regulatory RNAs in Virulence and Host-Microbe Interactions
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Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
/content/10.1128/9781683670247.chap18.fig18-1
Figure 1
Selection of virulence-associated regulatory RNA elements in human pathogens. Representatives of distinct classes of regulatory RNA are indicated (see color code on top). Illustrated are all RNAs referred to in the main text and in Table 1 ; absence of RNAs (e.g., CsrB/C) in a given pathogen does not necessarily imply that they are not encoded by that bacterium, but rather that they are not explicitly mentioned in the text. Several bacterial pathogens may colonize multiple niches and cause more than a single disease in their human host, but they are assigned to just one organ and illness here for the sake of simplicity. GAS, group A .
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Image of Figure 1
Figure 1

Selection of virulence-associated regulatory RNA elements in human pathogens. Representatives of distinct classes of regulatory RNA are indicated (see color code on top). Illustrated are all RNAs referred to in the main text and in Table 1 ; absence of RNAs (e.g., CsrB/C) in a given pathogen does not necessarily imply that they are not encoded by that bacterium, but rather that they are not explicitly mentioned in the text. Several bacterial pathogens may colonize multiple niches and cause more than a single disease in their human host, but they are assigned to just one organ and illness here for the sake of simplicity. GAS, group A .

Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
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Figure 2
Global RBPs contribute to virulence. (a) Virulence phenotypes associated with the deletion of the five major RBPs in Typhimurium: the RNA chaperones Hfq ( ) and ProQ ( ; Westermann et al., unpublished), the translational regulator CsrA ( ), and the cold shock proteins CspC and CspE ( ). The asterisk (*) indicates that the biofilm formation phenotype of Δ mutants stems from work with ( ). (b) The interactome of the same RBPs in Typhimurium is enriched for virulence-associated mRNAs. Gene ontology enrichment analysis ( ) on CLIP-seq data for Hfq and CsrA ( ) and RIP-seq data for ProQ ( ) and CspC and CspE ( ). Fold enrichments of all significantly enriched ( < 0.05) pathways are plotted. Virulence-related pathways are in bold.
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Figure 2

Global RBPs contribute to virulence. (a) Virulence phenotypes associated with the deletion of the five major RBPs in Typhimurium: the RNA chaperones Hfq ( ) and ProQ ( ; Westermann et al., unpublished), the translational regulator CsrA ( ), and the cold shock proteins CspC and CspE ( ). The asterisk (*) indicates that the biofilm formation phenotype of Δ mutants stems from work with ( ). (b) The interactome of the same RBPs in Typhimurium is enriched for virulence-associated mRNAs. Gene ontology enrichment analysis ( ) on CLIP-seq data for Hfq and CsrA ( ) and RIP-seq data for ProQ ( ) and CspC and CspE ( ). Fold enrichments of all significantly enriched ( < 0.05) pathways are plotted. Virulence-related pathways are in bold.

Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
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Figure 3
General lack of phenotypes of virulence-associated RNAs. An Rfam search ( ) for the query term “virulence” yielded 373 hits (as of February 2017). From these, nonbacterial RNAs and CRISPR RNAs were removed. For the remaining 308 entries, a manual literature search revealed whether or not the respective deletion/disruption mutants exhibit a virulence defect in cell culture ( phenotype), live-animal models (), or both.
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10.1128/9781683670247/fig18-3.gif
Image of Figure 3
Figure 3

General lack of phenotypes of virulence-associated RNAs. An Rfam search ( ) for the query term “virulence” yielded 373 hits (as of February 2017). From these, nonbacterial RNAs and CRISPR RNAs were removed. For the remaining 308 entries, a manual literature search revealed whether or not the respective deletion/disruption mutants exhibit a virulence defect in cell culture ( phenotype), live-animal models (), or both.

Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
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Figure 4
Common principles of sRNA-based virulence control. (a) The tight interconnection between metabolism and virulence is illustrated by the transcription of certain sRNAs in response to metabolic or infection-related cues, which in turn control virulence regulators/effectors, nutrient transporters, and/or metabolic enzymes. (b) Control of major lifestyle transitions. Upon sensing of a specific trigger, a bacterial sRNA may act in concert with transcription factors (not shown) to coordinate the rapid silencing of genes and degradation of mRNAs no longer needed under the new condition (circuit 1). This mechanism differs from feedback control, where sRNA and target are coactivated by the same stimulus (circuit 2). (c) sRNAs target mRNAs for key regulatory proteins, thereby indirectly controlling the expression of genes that are under the transcriptional control of those regulators. Often this RNA-based regulatory network ensures mutually exclusive activation of opposing processes (exemplified here by motility and virulence effector secretion). (d) Functional redundancy between sRNA homologs. sRNA pairs might arise from gene duplication events and thus share sequence homology, allowing the regulation of shared targets. However, functional redundancy might only be partial, when sibling sRNAs are produced under different conditions, interact with distinct cellular protein partners, or base-pair uniquely with specific mRNAs.
10.1128/9781683670247/fig18-4_thmb.gif
10.1128/9781683670247/fig18-4.gif
Image of Figure 4
Figure 4

Common principles of sRNA-based virulence control. (a) The tight interconnection between metabolism and virulence is illustrated by the transcription of certain sRNAs in response to metabolic or infection-related cues, which in turn control virulence regulators/effectors, nutrient transporters, and/or metabolic enzymes. (b) Control of major lifestyle transitions. Upon sensing of a specific trigger, a bacterial sRNA may act in concert with transcription factors (not shown) to coordinate the rapid silencing of genes and degradation of mRNAs no longer needed under the new condition (circuit 1). This mechanism differs from feedback control, where sRNA and target are coactivated by the same stimulus (circuit 2). (c) sRNAs target mRNAs for key regulatory proteins, thereby indirectly controlling the expression of genes that are under the transcriptional control of those regulators. Often this RNA-based regulatory network ensures mutually exclusive activation of opposing processes (exemplified here by motility and virulence effector secretion). (d) Functional redundancy between sRNA homologs. sRNA pairs might arise from gene duplication events and thus share sequence homology, allowing the regulation of shared targets. However, functional redundancy might only be partial, when sibling sRNAs are produced under different conditions, interact with distinct cellular protein partners, or base-pair uniquely with specific mRNAs.

Citation: Westermann A. 2019. Regulatory RNAs in Virulence and Host-Microbe Interactions, p 305-337. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0002-2017
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