1887

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

Author: Alexander J. Westermann1
VIEW AFFILIATIONS HIDE AFFILIATIONS
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

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Preview this chapter:
Preview Magnify
Zoom in
Zoomout

Regulatory RNAs in Virulence and Host-Microbe Interactions, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap18-1.gif /docserver/preview/fulltext/10.1128/9781683670247/9781683670230_Chap18-2.gif

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
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

Figures

Regulatory RNAs in Virulence and Host-Microbe Interactions
[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/author/10.1128/9781683670247.chap18-1,webId=/content/author/10.1128/9781683670247.chap18-1,properties={foaf_givenname=Alexander J., foaf_name=Alexander J. Westermann, foaf_surname=Westermann, pub_isAffiliatedWith=[com.pub2web.rdf.cci.facet.ContentItem[id=http://asm.metastore.ingenta.com/content/affiliation/10.1128/9781683670247.chap18-aff1]]}]]
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 .
10.1128/9781683670247/fig18-1_thmb.gif
10.1128/9781683670247/fig18-1.gif
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
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781683670247.chap18.fig18-2
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.
10.1128/9781683670247/fig18-2_thmb.gif
10.1128/9781683670247/fig18-2.gif
Image of Figure 2
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
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781683670247.chap18.fig18-3
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.
10.1128/9781683670247/fig18-3_thmb.gif
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
Permissions and Reprints Request Permissions
Download as Powerpoint
/content/10.1128/9781683670247.chap18.fig18-4
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.
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
Permissions and Reprints Request Permissions
Download as Powerpoint

References

/content/book/10.1128/9781683670247.chap18
1. Morens DM,, Fauci AS . 2013. Emerging infectious diseases: threats to human health and global stability. PLoS Pathog 9 : e1003467.[CrossRef][PubMed]
2. Breaker RR . 2012. Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4 : a003566.[CrossRef][PubMed]
3. Lasa I,, Toledo-Arana A,, Gingeras TR . 2012. An effort to make sense of antisense transcription in bacteria. RNA Biol 9 : 1039– 1044.[PubMed]
4. Wen Y,, Feng J,, Sachs G . 2013. Helicobacter pylori 5′ ureB-sRNA, a cis-encoded antisense small RNA, negatively regulates ureAB expression by transcription termination. J Bacteriol 195 : 444– 452.[PubMed]
5. Storz G,, Vogel J,, Wassarman KM . 2011. Regulation by small RNAs in bacteria: expanding frontiers. Mol Cell 43 : 880– 891.[PubMed]
6. Wagner EG,, Romby P . 2015. Small RNAs in bacteria and archaea: who they are, what they do, and how they do it. Adv Genet 90 : 133– 208.[PubMed]
7. Gottesman S,, Storz G . 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3 : a003798.[CrossRef][PubMed]
8. Holmqvist E,, Wagner EG . 2017. Impact of bacterial sRNAs in stress responses. Biochem Soc Trans 45 : 1203– 1212.[PubMed]
9. Toledo-Arana A,, Dussurget O,, Nikitas G,, Sesto N,, Guet-Revillet H,, Balestrino D,, Loh E,, Gripenland J,, Tiensuu T,, Vaitkevicius K,, Barthelemy M,, Vergassola M,, Nahori MA,, Soubigou G,, Régnault B,, Coppée JY,, Lecuit M,, Johansson J,, Cossart P . 2009. The Listeria transcriptional landscape from saprophytism to virulence. Nature 459 : 950– 956.[PubMed]
10. Sharma CM,, Hoffmann S,, Darfeuille F,, Reignier J,, Findeiss S,, Sittka A,, Chabas S,, Reiche K,, Hackermuller J,, Reinhardt R,, Stadler PF,, Vogel J . 2010. The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464 : 250– 255.[PubMed]
11. Albrecht M,, Sharma CM,, Dittrich MT,, Muller T,, Reinhardt R,, Vogel J,, Rudel T . 2011. The transcriptional landscape of Chlamydia pneumoniae. Genome Biol 12 : R98.[CrossRef][PubMed]
12. Kroger C,, Colgan A,, Srikumar S,, Handler K,, Sivasankaran SK,, Hammarlof DL,, Canals R,, Grissom JE,, Conway T,, Hokamp K,, Hinton JC . 2013. An infection-relevant transcriptomic compendium for Salmonella enterica serovar Typhimurium. Cell Host Microbe 14 : 683– 695.[PubMed]
13. Haning K,, Cho SH,, Contreras LM . 2014. Small RNAs in mycobacteria: an unfolding story. Front Cell Infect Microbiol 4 : 96.[CrossRef][PubMed]
14. Srikumar S,, Kroger C,, Hebrard M,, Colgan A,, Owen SV,, Sivasankaran SK,, Cameron AD,, Hokamp K,, Hinton JC . 2015. RNA-seq brings new insights to the intra-macrophage transcriptome of Salmonella Typhimurium. PLoS Pathog 11 : e1005262.[CrossRef][PubMed]
15. Nuss AM,, Beckstette M,, Pimenova M,, Schmuhl C,, Opitz W,, Pisano F,, Heroven AK,, Dersch P . 2017. Tissue dual RNA-seq allows fast discovery of infection-specific functions and riboregulators shaping host-pathogen transcriptomes. Proc Natl Acad Sci U S A 114 : E791– E800.[PubMed]
16. Papenfort K,, Vogel J . 2010. Regulatory RNA in bacterial pathogens. Cell Host Microbe 8 : 116– 127.[PubMed]
17. Gripenland J,, Netterling S,, Loh E,, Tiensuu T,, Toledo-Arana A,, Johansson J . 2010. RNAs: regulators of bacterial virulence. Nat Rev Microbiol 8 : 857– 866.[PubMed]
18. Caldelari I,, Chao Y,, Romby P,, Vogel J . 2013. RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb Perspect Med 3 : a010298.[CrossRef][PubMed]
19. Oliva G,, Sahr T,, Buchrieser C . 2015. Small RNAs, 5′ UTR elements and RNA-binding proteins in intracellular bacteria: impact on metabolism and virulence. FEMS Microbiol Rev 39 : 331– 349.[PubMed]
20. Svensson SL,, Sharma CM . 2016. Small RNAs in bacterial virulence and communication. Microbiol Spectr 4 : VMBF-0028-2015.[CrossRef]
21. Heroven AK,, Nuss AM,, Dersch P . 2017. RNA-based mechanisms of virulence control in Enterobacteriaceae. RNA Biol 14 : 471– 487.[PubMed]
22. Quereda JJ,, Cossart P . 2017. Regulating bacterial virulence with RNA. Annu Rev Microbiol 71 : 263– 280.[PubMed]
23. Somerville GA,, Proctor RA . 2009. At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci. Microbiol Mol Biol Rev 73 : 233– 248.[PubMed]
24. Sudarsan N,, Lee ER,, Weinberg Z,, Moy RH,, Kim JN,, Link KH,, Breaker RR . 2008. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 321 : 411– 413.[PubMed]
25. Lee ER,, Baker JL,, Weinberg Z,, Sudarsan N,, Breaker RR . 2010. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329 : 845– 848.[PubMed]
26. Miotto P,, Forti F,, Ambrosi A,, Pellin D,, Veiga DF,, Balazsi G,, Gennaro ML,, Di Serio C,, Ghisotti D,, Cirillo DM . 2012. Genome-wide discovery of small RNAs in Mycobacterium tuberculosis. PLoS One 7 : e51950.[CrossRef][PubMed]
27. Kortmann J,, Narberhaus F . 2012. Bacterial RNA thermometers: molecular zippers and switches. Nat Rev Microbiol 10 : 255– 265.[PubMed]
28. Hoe NP,, Goguen JD . 1993. Temperature sensing in Yersinia pestis: translation of the LcrF activator protein is thermally regulated. J Bacteriol 175 : 7901– 7909.
29. Bohme K,, Steinmann R,, Kortmann J,, Seekircher S,, Heroven AK,, Berger E,, Pisano F,, Thiermann T,, Wolf-Watz H,, Narberhaus F,, Dersch P . 2012. Concerted actions of a thermo-labile regulator and a unique intergenic RNA thermosensor control Yersinia virulence. PLoS Pathog 8 : e1002518.[CrossRef][PubMed]
30. Grosso-Becerra MV,, Croda-García G,, Merino E,, Servín-González L,, Mojica-Espinosa R,, Soberón-Chávez G . 2014. Regulation of Pseudomonas aeruginosa virulence factors by two novel RNA thermometers. Proc Natl Acad Sci U S A 111 : 15562– 15567.[PubMed]
31. Weber GG,, Kortmann J,, Narberhaus F,, Klose KE . 2014. RNA thermometer controls temperature-dependent virulence factor expression in Vibrio cholerae. Proc Natl Acad Sci U S A 111 : 14241– 14246.[PubMed]
32. Johansson J,, Mandin P,, Renzoni A,, Chiaruttini C,, Springer M,, Cossart P . 2002. An RNA thermosensor controls expression of virulence genes in Listeria monocytogenes. Cell 110 : 551– 561.
33. Loh E,, Kugelberg E,, Tracy A,, Zhang Q,, Gollan B,, Ewles H,, Chalmers R,, Pelicic V,, Tang CM . 2013. Temperature triggers immune evasion by Neisseria meningitidis. Nature 502 : 237– 240.[PubMed]
34. Bingham RJ,, Hall KS,, Slonczewski JL . 1990. Alkaline induction of a novel gene locus, alx, in Escherichia coli. J Bacteriol 172 : 2184– 2186.[PubMed]
35. Stancik LM,, Stancik DM,, Schmidt B,, Barnhart DM,, Yoncheva YN,, Slonczewski JL . 2002. pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol 184 : 4246– 4258.[PubMed]
36. Nechooshtan G,, Elgrably-Weiss M,, Sheaffer A,, Westhof E,, Altuvia S . 2009. A pH-responsive riboregulator. Genes Dev 23 : 2650– 2662.[PubMed]
37. Groisman EA . 2001. The pleiotropic two-component regulatory system PhoP-PhoQ. J Bacteriol 183 : 1835– 1842.[PubMed]
38. Hautefort I,, Thompson A,, Eriksson-Ygberg S,, Parker ML,, Lucchini S,, Danino V,, Bongaerts RJ,, Ahmad N,, Rhen M,, Hinton JC . 2008. During infection of epithelial cells Salmonella enterica serovar Typhimurium undergoes a time-dependent transcriptional adaptation that results in simultaneous expression of three type 3 secretion systems. Cell Microbiol 10 : 958– 984.[PubMed]
39. Blanc-Potard AB,, Groisman EA . 1997. The SalmonellaselC locus contains a pathogenicity island mediating intramacrophage survival. EMBO J 16 : 5376– 5385.[PubMed]
40. Lee EJ,, Groisman EA . 2012. Control of a Salmonella virulence locus by an ATP-sensing leader messenger RNA. Nature 486 : 271– 275.[PubMed]
41. Lee EJ,, Choi J,, Groisman EA . 2014. Control of a Salmonella virulence operon by proline-charged tRNA Pro. Proc Natl Acad Sci U S A 111 : 3140– 3145.[PubMed]
42. Lee EJ,, Groisman EA . 2010. An antisense RNA that governs the expression kinetics of a multifunctional virulence gene. Mol Microbiol 76 : 1020– 1033.[PubMed]
43. Choi E,, Han Y,, Cho YJ,, Nam D,, Lee EJ . 2017. A trans-acting leader RNA from a Salmonella virulence gene. Proc Natl Acad Sci U S A 114 : 10232– 10237.[PubMed]
44. Lee JW,, Lee EJ . 2015. Regulation and function of the Salmonella MgtC virulence protein. J Microbiol 53 : 667– 672.[PubMed]
45. Wagner EG,, Simons RW . 1994. Antisense RNA control in bacteria, phages, and plasmids. Annu Rev Microbiol 48 : 713– 742.[PubMed]
46. Georg J,, Hess WR . 2011. cis-antisense RNA, another level of gene regulation in bacteria. Microbiol Mol Biol Rev 75 : 286– 300.[PubMed]
47. Lybecker M,, Bilusic I,, Raghavan R . 2014. Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5 : e944039.[CrossRef][PubMed]
48. Raghavan R,, Sloan DB,, Ochman H . 2012. Antisense transcription is pervasive but rarely conserved in enteric bacteria. mBio 3 : e00156-12.[CrossRef][PubMed]
49. Lloréns-Rico V,, Cano J,, Kamminga T,, Gil R,, Latorre A,, Chen WH,, Bork P,, Glass JI,, Serrano L,, Lluch-Senar M . 2016. Bacterial antisense RNAs are mainly the product of transcriptional noise. Sci Adv 2 : e1501363.[CrossRef][PubMed]
50. Belzer C,, van Schendel BA,, Kuipers EJ,, Kusters JG,, van Vliet AH . 2007. Iron-responsive repression of urease expression in Helicobacter hepaticus is mediated by the transcriptional regulator Fur. Infect Immun 75 : 745– 752.[PubMed]
51. Wen Y,, Feng J,, Scott DR,, Marcus EA,, Sachs G . 2011. A cis-encoded antisense small RNA regulated by the HP0165-HP0166 two-component system controls expression of ureB in Helicobacter pylori. J Bacteriol 193 : 40– 51.[PubMed]
52. Oliva G,, Sahr T,, Rolando M,, Knoth M,, Buchrieser C . 2017. A unique cis-encoded small noncoding RNA is regulating Legionella pneumophila Hfq expression in a life cycle-dependent manner. mBio 3 : e02182-16.[CrossRef]
53. Grundling A,, Burrack LS,, Bouwer HG,, Higgins DE . 2004. Listeria monocytogenes regulates flagellar motility gene expression through MogR, a transcriptional repressor required for virulence. Proc Natl Acad Sci U S A 101 : 12318– 12323.[PubMed]
54. Wurtzel O,, Sesto N,, Mellin JR,, Karunker I,, Edelheit S,, Bécavin C,, Archambaud C,, Cossart P,, Sorek R . 2012. Comparative transcriptomics of pathogenic and non-pathogenic Listeria species. Mol Syst Biol 8 : 583.[CrossRef][PubMed]
55. Schultze T,, Hilker R,, Mannala GK,, Gentil K,, Weigel M,, Farmani N,, Windhorst AC,, Goesmann A,, Chakraborty T,, Hain T . 2015. A detailed view of the intracellular transcriptome of Listeria monocytogenes in murine macrophages using RNA-seq. Front Microbiol 6 : 1199.[CrossRef][PubMed]
56. Sesto N,, Wurtzel O,, Archambaud C,, Sorek R,, Cossart P . 2013. The excludon: a new concept in bacterial antisense RNA-mediated gene regulation. Nat Rev Microbiol 11 : 75– 82.[PubMed]
57. Yamaguchi Y,, Park JH,, Inouye M . 2011. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45 : 61– 79.[PubMed]
58. Berghoff BA,, Wagner EG . 2017. RNA-based regulation in type I toxin-antitoxin systems and its implication for bacterial persistence. Curr Genet 63 : 1011– 1016.[PubMed]
59. Page R,, Peti W . 2016. Toxin-antitoxin systems in bacterial growth arrest and persistence. Nat Chem Biol 12 : 208– 214.[PubMed]
60. Arnion H,, Korkut DN,, Masachis Gelo S,, Chabas S,, Reignier J,, Iost I,, Darfeuille F . 2017. Mechanistic insights into type I toxin antitoxin systems in Helicobacter pylori: the importance of mRNA folding in controlling toxin expression. Nucleic Acids Res 45 : 4782– 4795.[PubMed]
61. Vogel J,, Argaman L,, Wagner EG,, Altuvia S . 2004. The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14 : 2271– 2276.[PubMed]
62. Berghoff BA,, Hoekzema M,, Aulbach L,, Wagner EG . 2017. Two regulatory RNA elements affect TisB-dependent depolarization and persister formation. Mol Microbiol 103 : 1020– 1033.[PubMed]
63. Beaume M,, Hernandez D,, Farinelli L,, Deluen C,, Linder P,, Gaspin C,, Romby P,, Schrenzel J,, Francois P . 2010. Cartography of methicillin-resistant S. aureus transcripts: detection, orientation and temporal expression during growth phase and stress conditions. PLoS One 5 : e10725.[CrossRef][PubMed]
64. Sayed N,, Jousselin A,, Felden B . 2011. A cis-antisense RNA acts in trans in Staphylococcus aureus to control translation of a human cytolytic peptide. Nat Struct Mol Biol 19 : 105– 112.[PubMed]
65. Jorgensen MG,, Thomason MK,, Havelund J,, Valentin-Hansen P,, Storz G . 2013. Dual function of the McaS small RNA in controlling biofilm formation. Genes Dev 27 : 1132– 1145.[PubMed]
66. Holmqvist E,, Vogel J . 2013. A small RNA serving both the Hfq and CsrA regulons. Genes Dev 27 : 1073– 1078.[PubMed]
67. Romeo T . 1998. Global regulation by the small RNA-binding protein CsrA and the non-coding RNA molecule CsrB. Mol Microbiol 29 : 1321– 1330.[PubMed]
68. Babitzke P,, Romeo T . 2007. CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10 : 156– 163.[PubMed]
69. Martínez LC,, Yakhnin H,, Camacho MI,, Georgellis D,, Babitzke P,, Puente JL,, Bustamante VH . 2011. Integration of a complex regulatory cascade involving the SirA/BarA and Csr global regulatory systems that controls expression of the Salmonella SPI-1 and SPI-2 virulence regulons through HilD. Mol Microbiol 80 : 1637– 1656.[PubMed]
70. Heroven AK,, Böhme K,, Dersch P . 2012. The Csr/Rsm system of Yersinia and related pathogens: a post-transcriptional strategy for managing virulence. RNA Biol 9 : 379– 391.[PubMed]
71. Gore AL,, Payne SM . 2010. CsrA and Cra influence Shigella flexneri pathogenesis. Infect Immun 78 : 4674– 4682.[PubMed]
72. Sahr T,, Brüggemann H,, Jules M,, Lomma M,, Albert-Weissenberger C,, Cazalet C,, Buchrieser C . 2009. Two small ncRNAs jointly govern virulence and transmission in Legionella pneumophila. Mol Microbiol 72 : 741– 762.[PubMed]
73. Wassarman KM . 2007. 6S RNA: a small RNA regulator of transcription. Curr Opin Microbiol 10 : 164– 168.[PubMed]
74. Barrick JE,, Sudarsan N,, Weinberg Z,, Ruzzo WL,, Breaker RR . 2005. 6S RNA is a widespread regulator of eubacterial RNA polymerase that resembles an open promoter. RNA 11 : 774– 784.[PubMed]
75. Faucher SP,, Friedlander G,, Livny J,, Margalit H,, Shuman HA . 2010. Legionella pneumophila 6S RNA optimizes intracellular multiplication. Proc Natl Acad Sci U S A 107 : 7533– 7538.[PubMed]
76. Thiennimitr P,, Winter SE,, Winter MG,, Xavier MN,, Tolstikov V,, Huseby DL,, Sterzenbach T,, Tsolis RM,, Roth JR,, Bäumler AJ . 2011. Intestinal inflammation allows Salmonella to use ethanolamine to compete with the microbiota. Proc Natl Acad Sci U S A 108 : 17480– 17485.[PubMed]
77. Mellin JR,, Koutero M,, Dar D,, Nahori MA,, Sorek R,, Cossart P . 2014. Riboswitches. Sequestration of a two-component response regulator by a riboswitch-regulated noncoding RNA. Science 345 : 940– 943.[PubMed]
78. DebRoy S,, Gebbie M,, Ramesh A,, Goodson JR,, Cruz MR,, van Hoof A,, Winkler WC,, Garsin DA,, DebRoy S . 2014. Riboswitches. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator. Science 345 : 937– 940.[PubMed]
79. Song T,, Mika F,, Lindmark B,, Liu Z,, Schild S,, Bishop A,, Zhu J,, Camilli A,, Johansson J,, Vogel J,, Wai SN . 2008. A new Vibrio cholerae sRNA modulates colonization and affects release of outer membrane vesicles. Mol Microbiol 70 : 100– 111.[PubMed]
80. Song T,, Sabharwal D,, Wai SN . 2010. VrrA mediates Hfq-dependent regulation of OmpT synthesis in Vibrio cholerae. J Mol Biol 400 : 682– 688.[PubMed]
81. Ng WL,, Bassler BL . 2009. Bacterial quorum-sensing network architectures. Annu Rev Genet 43 : 197– 222.[PubMed]
82. Bardill JP,, Zhao X,, Hammer BK . 2011. The Vibrio cholerae quorum sensing response is mediated by Hfq-dependent sRNA/mRNA base pairing interactions. Mol Microbiol 80 : 1381– 1394.[PubMed]
83. Shao Y,, Bassler BL . 2014. Quorum regulatory small RNAs repress type VI secretion in Vibrio cholerae. Mol Microbiol 92 : 921– 930.[PubMed]
84. Richard AL,, Withey JH,, Beyhan S,, Yildiz F,, DiRita VJ . 2010. The Vibrio cholerae virulence regulatory cascade controls glucose uptake through activation of TarA, a small regulatory RNA. Mol Microbiol 78 : 1171– 1181.[PubMed]
85. Bradley ES,, Bodi K,, Ismail AM,, Camilli A . 2011. A genome-wide approach to discovery of small RNAs involved in regulation of virulence in Vibrio cholerae. PLoS Pathog 7 : e1002126.[CrossRef][PubMed]
86. Davies BW,, Bogard RW,, Young TS,, Mekalanos JJ . 2012. Coordinated regulation of accessory genetic elements produces cyclic di-nucleotides for V. cholerae virulence. Cell 149 : 358– 370.[PubMed]
87. Papenfort K,, Forstner KU,, Cong JP,, Sharma CM,, Bassler BL . 2015. Differential RNA-seq of Vibrio cholerae identifies the VqmR small RNA as a regulator of biofilm formation. Proc Natl Acad Sci U S A 112 : E766– E775.[PubMed]
88. Papenfort K,, Silpe JE,, Schramma KR,, Cong JP,, Seyedsayamdost MR,, Bassler BL . 2017. A Vibrio cholerae autoinducer-receptor pair that controls biofilm formation. Nat Chem Biol 13 : 551– 557.[PubMed]
89. Miller MB,, Skorupski K,, Lenz DH,, Taylor RK,, Bassler BL . 2002. Parallel quorum sensing systems converge to regulate virulence in Vibrio cholerae. Cell 110 : 303– 314.
90. Zhu J,, Miller MB,, Vance RE,, Dziejman M,, Bassler BL,, Mekalanos JJ . 2002. Quorum-sensing regulators control virulence gene expression in Vibrio cholerae. Proc Natl Acad Sci U S A 99 : 3129– 3134.[PubMed]
91. Pfeiffer V,, Sittka A,, Tomer R,, Tedin K,, Brinkmann V,, Vogel J . 2007. A small non-coding RNA of the invasion gene island (SPI-1) represses outer membrane protein synthesis from the Salmonella core genome. Mol Microbiol 66 : 1174– 1191.[PubMed]
92. Song M,, Sukovich DJ,, Ciccarelli L,, Mayr J,, Fernandez-Rodriguez J,, Mirsky EA,, Tucker AC,, Gordon DB,, Marlovits TC,, Voigt CA . 2017. Control of type III protein secretion using a minimal genetic system. Nat Commun 8 : 14737.[CrossRef][PubMed]
93. Padalon-Brauch G,, Hershberg R,, Elgrably-Weiss M,, Baruch K,, Rosenshine I,, Margalit H,, Altuvia S . 2008. Small RNAs encoded within genetic islands of Salmonella typhimurium show host-induced expression and role in virulence. Nucleic Acids Res 36 : 1913– 1927.[PubMed]
94. Gong H,, Vu GP,, Bai Y,, Chan E,, Wu R,, Yang E,, Liu F,, Lu S . 2011. A Salmonella small non-coding RNA facilitates bacterial invasion and intracellular replication by modulating the expression of virulence factors. PLoS Pathog 7 : e1002120.[CrossRef][PubMed]
95. Westermann AJ,, Förstner KU,, Amman F,, Barquist L,, Chao Y,, Schulte LN,, Müller L,, Reinhardt R,, Stadler PF,, Vogel J . 2016. Dual RNA-seq unveils noncoding RNA functions in host-pathogen interactions. Nature 529 : 496– 501.[PubMed]
96. Chaudhuri RR,, Morgan E,, Peters SE,, Pleasance SJ,, Hudson DL,, Davies HM,, Wang J,, van Diemen PM,, Buckley AM,, Bowen AJ,, Pullinger GD,, Turner DJ,, Langridge GC,, Turner AK,, Parkhill J,, Charles IG,, Maskell DJ,, Stevens MP . 2013. Comprehensive assignment of roles for Salmonella typhimurium genes in intestinal colonization of food-producing animals. PLoS Genet 9 : e1003456.[CrossRef][PubMed]
97. Grieshaber NA,, Grieshaber SS,, Fischer ER,, Hackstadt T . 2006. A small RNA inhibits translation of the histone-like protein Hc1 in Chlamydia trachomatis. Mol Microbiol 59 : 541– 550.[PubMed]
98. Khandige S,, Kronborg T,, Uhlin BE,, Møller-Jensen J . 2015. sRNA-mediated regulation of P-fimbriae phase variation in uropathogenic Escherichia coli. PLoS Pathog 11 : e1005109.[CrossRef][PubMed]
99. Mellin JR,, Goswami S,, Grogan S,, Tjaden B,, Genco CA . 2007. A novel Fur- and iron-regulated small RNA, NrrF, is required for indirect Fur-mediated regulation of the sdhA and sdhC genes in Neisseria meningitidis. J Bacteriol 189 : 3686– 3694.[PubMed]
100. Mellin JR,, McClure R,, Lopez D,, Green O,, Reinhard B,, Genco C . 2010. Role of Hfq in iron-dependent and -independent gene regulation in Neisseria meningitidis. Microbiology 156 : 2316– 2326.[PubMed]
101. Heidrich N,, Bauriedl S,, Barquist L,, Li L,, Schoen C,, Vogel J . 2017. The primary transcriptome of Neisseria meningitidis and its interaction with the RNA chaperone Hfq. Nucleic Acids Res 45 : 6147– 6167.[PubMed]
102. Pannekoek Y,, Huis In ’t Veld RA,, Schipper K,, Bovenkerk S,, Kramer G,, Brouwer MC,, van de Beek D,, Speijer D,, van der Ende A . 2017. Neisseria meningitidis uses sibling small regulatory RNAs to switch from cataplerotic to anaplerotic metabolism. mBio 8 : e02293-16.[CrossRef][PubMed]
103. Romilly C,, Lays C,, Tomasini A,, Caldelari I,, Benito Y,, Hammann P,, Geissmann T,, Boisset S,, Romby P,, Vandenesch F . 2014. A non-coding RNA promotes bacterial persistence and decreases virulence by regulating a regulator in Staphylococcus aureus. PLoS Pathog 10 : e1003979.[CrossRef][PubMed]
104. Roberts SA,, Scott JR . 2007. RivR and the small RNA RivX: the missing links between the CovR regulatory cascade and the Mga regulon. Mol Microbiol 66 : 1506– 1522.
105. Morfeldt E,, Taylor D,, von Gabain A,, Arvidson S . 1995. Activation of alpha-toxin translation in Staphylococcus aureus by the trans-encoded antisense RNA, RNAIII. EMBO J 14 : 4569– 4577.[PubMed]
106. Fröhlich KS,, Vogel J . 2009. Activation of gene expression by small RNA. Curr Opin Microbiol 12 : 674– 682.[PubMed]
107. Quereda JJ,, Ortega AD,, Pucciarelli MG,, García-Del Portillo F . 2014. The Listeria small RNA Rli27 regulates a cell wall protein inside eukaryotic cells by targeting a long 5′-UTR variant. PLoS Genet 10 : e1004765.[CrossRef][PubMed]
108. Ramirez-Peña E,, Treviño J,, Liu Z,, Perez N,, Sumby P . 2010. The group A Streptococcus small regulatory RNA FasX enhances streptokinase activity by increasing the stability of the ska mRNA transcript. Mol Microbiol 78 : 1332– 1347.[PubMed]
109. Liu Z,, Treviño J,, Ramirez-Peña E,, Sumby P . 2012. The small regulatory RNA FasX controls pilus expression and adherence in the human bacterial pathogen group A Streptococcus. Mol Microbiol 86 : 140– 154.[PubMed]
110. Danger JL,, Cao TN,, Cao TH,, Sarkar P,, Treviño J,, Pflughoeft KJ,, Sumby P . 2015. The small regulatory RNA FasX enhances group A Streptococcus virulence and inhibits pilus expression via serotype-specific targets. Mol Microbiol 96 : 249– 262.[PubMed]
111. Vandenesch F,, Kornblum J,, Novick RP . 1991. A temporal signal, independent of agr, is required for hla but not spa transcription in Staphylococcus aureus. J Bacteriol 173 : 6313– 6320.[PubMed]
112. Novick RP . 2003. Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48 : 1429– 1449.[PubMed]
113. Boisset S,, Geissmann T,, Huntzinger E,, Fechter P,, Bendridi N,, Possedko M,, Chevalier C,, Helfer AC,, Benito Y,, Jacquier A,, Gaspin C,, Vandenesch F,, Romby P . 2007. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism. Genes Dev 21 : 1353– 1366.[PubMed]
114. Pernitzsch SR,, Tirier SM,, Beier D,, Sharma CM . 2014. A variable homopolymeric G-repeat defines small RNA-mediated posttranscriptional regulation of a chemotaxis receptor in Helicobacter pylori. Proc Natl Acad Sci U S A 111 : E501– E510.[PubMed]
115. Feng L,, Rutherford ST,, Papenfort K,, Bagert JD,, van Kessel JC,, Tirrell DA,, Wingreen NS,, Bassler BL . 2015. A Qrr noncoding RNA deploys four different regulatory mechanisms to optimize quorum-sensing dynamics. Cell 160 : 228– 240.[PubMed]
116. Vogel J,, Sharma CM . 2005. How to find small non-coding RNAs in bacteria. Biol Chem 386 : 1219– 1238.[PubMed]
117. Winkler WC,, Nahvi A,, Sudarsan N,, Barrick JE,, Breaker RR . 2003. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Biol 10 : 701– 707.[PubMed]
118. Loh E,, Dussurget O,, Gripenland J,, Vaitkevicius K,, Tiensuu T,, Mandin P,, Repoila F,, Buchrieser C,, Cossart P,, Johansson J . 2009. A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139 : 770– 779.[PubMed]
119. Ellis MJ,, Trussler RS,, Charles O,, Haniford DB . 2017. A transposon-derived small RNA regulates gene expression in Salmonella Typhimurium. Nucleic Acids Res 45 : 5470– 5486.[PubMed]
120. Ellis MJ,, Carfrae LA,, Macnair CR,, Trussler RS,, Brown ED,, Haniford DB . 2018. Silent but deadly: IS200 promotes pathogenicity in Salmonella Typhimurium. RNA Biol 15 : 176– 181.[PubMed]
121. Chao Y,, Papenfort K,, Reinhardt R,, Sharma CM,, Vogel J . 2012. An atlas of Hfq-bound transcripts reveals 3′ UTRs as a genomic reservoir of regulatory small RNAs. EMBO J 31 : 4005– 4019.[PubMed]
122. Miyakoshi M,, Chao Y,, Vogel J . 2015. Regulatory small RNAs from the 3′ regions of bacterial mRNAs. Curr Opin Microbiol 24 : 132– 139.[PubMed]
123. Novick RP,, Geisinger E . 2008. Quorum sensing in staphylococci. Annu Rev Genet 42 : 541– 564.[PubMed]
124. Papenfort K,, Sun Y,, Miyakoshi M,, Vanderpool CK,, Vogel J . 2013. Small RNA-mediated activation of sugar phosphatase mRNA regulates glucose homeostasis. Cell 153 : 426– 437.[PubMed]
125. Papenfort K,, Podkaminski D,, Hinton JC,, Vogel J . 2012. The ancestral SgrS RNA discriminates horizontally acquired Salmonella mRNAs through a single G-U wobble pair. Proc Natl Acad Sci U S A 109 : E757– E764.[PubMed]
126. Lloyd CR,, Park S,, Fei J,, Vanderpool CK . 2017. The small protein SgrT controls transport activity of the glucose-specific phosphotransferase system. J Bacteriol 199 : e00869-16.[CrossRef][PubMed]
127. Marraffini LA . 2015. CRISPR-Cas immunity in prokaryotes. Nature 526 : 55– 61.[PubMed]
128. Sampson TR,, Saroj SD,, Llewellyn AC,, Tzeng YL,, Weiss DS . 2013. A CRISPR/Cas system mediates bacterial innate immune evasion and virulence. Nature 497 : 254– 257.[PubMed]
129. Dugar G,, Leenay RT,, Eisenbart SK,, Bischler T,, Aul BU,, Beisel CL,, Sharma CM . 2018. CRISPR RNA-dependent binding and cleavage of endogenous RNAs by the Campylobacter jejuni Cas9. Mol Cell 69 : 893– 905.[PubMed]
130. Louwen R,, Horst-Kreft D,, de Boer AG,, van der Graaf L,, de Knegt G,, Hamersma M,, Heikema AP,, Timms AR,, Jacobs BC,, Wagenaar JA,, Endtz HP,, van der Oost J,, Wells JM,, Nieuwenhuis EE,, van Vliet AH,, Willemsen PT,, van Baarlen P,, van Belkum A . 2013. A novel link between Campylobacter jejuni bacteriophage defence, virulence and Guillain-Barré syndrome. Eur J Clin Microbiol Infect Dis 32 : 207– 226.[PubMed]
131. Gunderson FF,, Cianciotto NP . 2013. The CRISPR-associated gene cas2 of Legionella pneumophila is required for intracellular infection of amoebae. mBio 4 : e00074-13.[CrossRef][PubMed]
132. Gunderson FF,, Mallama CA,, Fairbairn SG,, Cianciotto NP . 2015. Nuclease activity of Legionella pneumophila Cas2 promotes intracellular infection of amoebal host cells. Infect Immun 83 : 1008– 1018.[PubMed]
133. Sesto N,, Touchon M,, Andrade JM,, Kondo J,, Rocha EP,, Arraiano CM,, Archambaud C,, Westhof E,, Romby P,, Cossart P . 2014. A PNPase dependent CRISPR system in Listeria. PLoS Genet 10 : e1004065.[CrossRef][PubMed]
134. Dubey AK,, Baker CS,, Romeo T,, Babitzke P . 2005. RNA sequence and secondary structure participate in high-affinity CsrA-RNA interaction. RNA 11 : 1579– 1587.[PubMed]
135. Duss O,, Michel E,, Diarra dit Konté N,, Schubert M,, Allain FH . 2014. Molecular basis for the wide range of affinity found in Csr/Rsm protein-RNA recognition. Nucleic Acids Res 42 : 5332– 5346.[PubMed]
136. Holmqvist E,, Wright PR,, Li L,, Bischler T,, Barquist L,, Reinhardt R,, Backofen R,, Vogel J . 2016. Global RNA recognition patterns of post-transcriptional regulators Hfq and CsrA revealed by UV crosslinking in vivo. EMBO J 35 : 991– 1011.[PubMed]
137. Vakulskas CA,, Potts AH,, Babitzke P,, Ahmer BM,, Romeo T . 2015. Regulation of bacterial virulence by Csr (Rsm) systems. Microbiol Mol Biol Rev 79 : 193– 224.[PubMed]
138. Lawhon SD,, Frye JG,, Suyemoto M,, Porwollik S,, McClelland M,, Altier C . 2003. Global regulation by CsrA in Salmonella typhimurium. Mol Microbiol 48 : 1633– 1645.[PubMed]
139. Kusmierek M,, Dersch P . 2017. Regulation of host-pathogen interactions via the post-transcriptional Csr/Rsm system. Curr Opin Microbiol 41 : 58– 67.[PubMed]
140. Bhatt S,, Edwards AN,, Nguyen HT,, Merlin D,, Romeo T,, Kalman D . 2009. The RNA binding protein CsrA is a pleiotropic regulator of the locus of enterocyte effacement pathogenicity island of enteropathogenic Escherichia coli. Infect Immun 77 : 3552– 3568.[PubMed]
141. Sahr T,, Rusniok C,, Impens F,, Oliva G,, Sismeiro O,, Coppée JY,, Buchrieser C . 2017. The Legionella pneumophila genome evolved to accommodate multiple regulatory mechanisms controlled by the CsrA-system. PLoS Genet 13 : e1006629.[CrossRef][PubMed]
142. Dugar G,, Svensson SL,, Bischler T,, Wäldchen S,, Reinhardt R,, Sauer M,, Sharma CM . 2016. The CsrA-FliW network controls polar localization of the dual-function flagellin mRNA in Campylobacter jejuni. Nat Commun 7 : 11667.[CrossRef][PubMed]
143. Fields JA,, Li J,, Gulbronson CJ,, Hendrixson DR,, Thompson SA . 2016. Campylobacter jejuni CsrA regulates metabolic and virulence associated proteins and is necessary for mouse colonization. PLoS One 11 : e0156932.[CrossRef][PubMed]
144. Vogel J,, Luisi BF . 2011. Hfq and its constellation of RNA. Nat Rev Microbiol 9 : 578– 589.[PubMed]
145. Peng Y,, Curtis JE,, Fang X,, Woodson SA . 2014. Structural model of an mRNA in complex with the bacterial chaperone Hfq. Proc Natl Acad Sci U S A 111 : 17134– 17139.[PubMed]
146. Santiago-Frangos A,, Kavita K,, Schu DJ,, Gottesman S,, Woodson SA . 2016. C-terminal domain of the RNA chaperone Hfq drives sRNA competition and release of target RNA. Proc Natl Acad Sci U S A 113 : E6089– E6096.[PubMed]
147. Chao Y,, Vogel J . 2010. The role of Hfq in bacterial pathogens. Curr Opin Microbiol 13 : 24– 33.[PubMed]
148. Sittka A,, Lucchini S,, Papenfort K,, Sharma CM,, Rolle K,, Binnewies TT,, Hinton JC,, Vogel J . 2008. Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4 : e1000163.[CrossRef][PubMed]
149. Tree JJ,, Granneman S,, McAteer SP,, Tollervey D,, Gally DL . 2014. Identification of bacteriophage-encoded anti-sRNAs in pathogenic Escherichia coli. Mol Cell 55 : 199– 213.[PubMed]
150. Christiansen JK,, Nielsen JS,, Ebersbach T,, Valentin-Hansen P,, Sogaard-Andersen L,, Kallipolitis BH . 2006. Identification of small Hfq-binding RNAs in Listeria monocytogenes. RNA 12 : 1383– 1396.[PubMed]
151. Sonnleitner E,, Sorger-Domenigg T,, Madej MJ,, Findeiss S,, Hackermüller J,, Hüttenhofer A,, Stadler PF,, Bläsi U,, Moll I . 2008. Detection of small RNAs in Pseudomonas aeruginosa by RNomics and structure-based bioinformatic tools. Microbiology 154 : 3175– 3187.[PubMed]
152. Möller P,, Overlöper A,, Förstner KU,, Wen TN,, Sharma CM,, Lai EM,, Narberhaus F . 2014. Profound impact of Hfq on nutrient acquisition, metabolism and motility in the plant pathogen Agrobacterium tumefaciens. PLoS One 9 : e110427.[CrossRef][PubMed]
153. Sonnleitner E,, Bläsi U . 2014. Regulation of Hfq by the RNA CrcZ in Pseudomonas aeruginosa carbon catabolite repression. PLoS Genet 10 : e1004440.[CrossRef][PubMed]
154. Ellis MJ,, Trussler RS,, Haniford DB . 2015. Hfq binds directly to the ribosome-binding site of IS 10 transposase mRNA to inhibit translation. Mol Microbiol 96 : 633– 650.[PubMed]
155. Chen J,, Gottesman S . 2017. Hfq links translation repression to stress-induced mutagenesis in E. coli. Genes Dev 31 : 1382– 1395.[PubMed]
156. Olejniczak M,, Storz G . 2017. ProQ/FinO-domain proteins: another ubiquitous family of RNA matchmakers? Mol Microbiol 104 : 905– 915.[PubMed]
157. Gonzalez GM,, Hardwick SW,, Maslen SL,, Skehel JM,, Holmqvist E,, Vogel J,, Bateman A,, Luisi BF,, Broadhurst RW . 2017. Structure of the Escherichia coli ProQ RNA-binding protein. RNA 23 : 696– 711.[PubMed]
158. Smirnov A,, Förstner KU,, Holmqvist E,, Otto A,, Guünster R,, Becher D,, Reinhardt R,, Vogel J . 2016. Grad-seq guides the discovery of ProQ as a major small RNA-binding protein. Proc Natl Acad Sci U S A 113 : 11591– 11596.[PubMed]
159. Attaiech L,, Boughammoura A,, Brochier-Armanet C,, Allatif O,, Peillard-Fiorente F,, Edwards RA,, Omar AR,, MacMillan AM,, Glover M,, Charpentier X . 2016. Silencing of natural transformation by an RNA chaperone and a multitarget small RNA. Proc Natl Acad Sci U S A 113 : 8813– 8818.[PubMed]
160. Smirnov A,, Wang C,, Drewry LL,, Vogel J . 2017. Molecular mechanism of mRNA repression in trans by a ProQ-dependent small RNA. EMBO J 36 : 1029– 1045.[PubMed]
161. Sheidy DT,, Zielke RA . 2013. Analysis and expansion of the role of the Escherichia coli protein ProQ. PLoS One 8 : e79656.[CrossRef][PubMed]
162. Michaux C,, Holmqvist E,, Vasicek E,, Sharan M,, Barquist L,, Westermann AJ,, Gunn JS,, Vogel J . 2017. RNA target profiles direct the discovery of virulence functions for the cold-shock proteins CspC and CspE. Proc Natl Acad Sci U S A 114 : 6824– 6829.
163. Beckmann BM,, Horos R,, Fischer B,, Castello A,, Eichelbaum K,, Alleaume AM,, Schwarzl T,, Curk T,, Foehr S,, Huber W,, Krijgsveld J,, Hentze MW . 2015. The RNA-binding proteomes from yeast to man harbour conserved enigmRBPs. Nat Commun 6 : 10127.[CrossRef][PubMed]
164. Mitobe J,, Yanagihara I,, Ohnishi K,, Yamamoto S,, Ohnishi M,, Ishihama A,, Watanabe H . 2011. RodZ regulates the post-transcriptional processing of the Shigella sonnei type III secretion system. EMBO Rep 12 : 911– 916.[PubMed]
165. Matos RG,, Casinhas J,, Bárria C,, Dos Santos RF,, Silva IJ,, Arraiano CM . 2017. The role of ribonucleases and sRNAs in the virulence of foodborne pathogens. Front Microbiol 8 : 910.[CrossRef][PubMed]
166. Mackie GA . 2013. RNase E: at the interface of bacterial RNA processing and decay. Nat Rev Microbiol 11 : 45– 57.[PubMed]
167. Yang J,, Jain C,, Schesser K . 2008. RNase E regulates the Yersinia type 3 secretion system. J Bacteriol 190 : 3774– 3778.[PubMed]
168. Schiano CA,, Bellows LE,, Lathem WW . 2010. The small RNA chaperone Hfq is required for the virulence of Yersinia pseudotuberculosis. Infect Immun 78 : 2034– 2044.[PubMed]
169. Rosenzweig JA,, Weltman G,, Plano GV,, Schesser K . 2005. Modulation of Yersinia type three secretion system by the S1 domain of polynucleotide phosphorylase. J Biol Chem 280 : 156– 163.[PubMed]
170. Rosenzweig JA,, Chromy B,, Echeverry A,, Yang J,, Adkins B,, Plano GV,, McCutchen-Maloney S,, Schesser K . 2007. Polynucleotide phosphorylase independently controls virulence factor expression levels and export in Yersinia spp. FEMS Microbiol Lett 270 : 255– 264.[PubMed]
171. Clements MO,, Eriksson S,, Thompson A,, Lucchini S,, Hinton JC,, Normark S,, Rhen M . 2002. Polynucleotide phosphorylase is a global regulator of virulence and persistency in Salmonella enterica. Proc Natl Acad Sci U S A 99 : 8784– 8789.[PubMed]
172. Ygberg SE,, Clements MO,, Rytkonen A,, Thompson A,, Holden DW,, Hinton JC,, Rhen M . 2006. Polynucleotide phosphorylase negatively controls spv virulence gene expression in Salmonella enterica. Infect Immun 74 : 1243– 1254.[PubMed]
173. Haddad N,, Tresse O,, Rivoal K,, Chevret D,, Nonglaton Q,, Burns CM,, Prévost H,, Cappelier JM . 2012. Polynucleotide phosphorylase has an impact on cell biology of Campylobacter jejuni. Front Cell Infect Microbiol 2 : 30.[CrossRef][PubMed]
174. Chevalier C,, Huntzinger E,, Fechter P,, Boisset S,, Vandenesch F,, Romby P,, Geissmann T . 2008. Staphylococcus aureus endoribonuclease III purification and properties. Methods Enzymol 447 : 309– 327.
175. Viegas SC,, Mil-Homens D,, Fialho AM,, Arraiano CM . 2013. The virulence of Salmonella enterica serovar Typhimurium in the insect model Galleria mellonella is impaired by mutations in RNase E and RNase III. Appl Environ Microbiol 79 : 6124– 6133.[PubMed]
176. Cheng ZF,, Zuo Y,, Li Z,, Rudd KE,, Deutscher MP . 1998. The vacB gene required for virulence in Shigella flexneri and Escherichia coli encodes the exoribonuclease RNase R. J Biol Chem 273 : 14077– 14080.[PubMed]
177. Leskinen K,, Varjosalo M,, Skurnik M . 2015. Absence of YbeY RNase compromises the growth and enhances the virulence plasmid gene expression of Yersinia enterocolitica O:3. Microbiology 161 : 285– 299.[PubMed]
178. Vercruysse M,, Köhrer C,, Davies BW,, Arnold MF,, Mekalanos JJ,, RajBhandary UL,, Walker GC . 2014. The highly conserved bacterial RNase YbeY is essential in Vibrio cholerae, playing a critical role in virulence, stress regulation, and RNA processing. PLoS Pathog 10 : e1004175.[CrossRef][PubMed]
179. Bigot A,, Raynaud C,, Dubail I,, Dupuis M,, Hossain H,, Hain T,, Chakraborty T,, Charbit A . 2009. lmo1273, a novel gene involved in Listeria monocytogenes virulence. Microbiology 155 : 891– 902.[PubMed]
180. Bugrysheva JV,, Scott JR . 2010. The ribonucleases J1 and J2 are essential for growth and have independent roles in mRNA decay in Streptococcus pyogenes. Mol Microbiol 75 : 731– 743.[PubMed]
181. Kaito C,, Kurokawa K,, Matsumoto Y,, Terao Y,, Kawabata S,, Hamada S,, Sekimizu K . 2005. Silkworm pathogenic bacteria infection model for identification of novel virulence genes. Mol Microbiol 56 : 934– 944.[PubMed]
182. Barquist L,, Vogel J . 2015. Accelerating discovery and functional analysis of small RNAs with new technologies. Annu Rev Genet 49 : 367– 394.[PubMed]
183. Hör J,, Gorski SA,, Vogel J . 2018. Bacterial RNA biology on a genome scale. Mol Cell.[CrossRef][PubMed]
184. Weinberg Z,, Wang JX,, Bogue J,, Yang J,, Corbino K,, Moy RH,, Breaker RR . 2010. Comparative genomics reveals 104 candidate structured RNAs from bacteria, archaea, and their metagenomes. Genome Biol 11 : R31.[CrossRef][PubMed]
185. Merino EJ,, Wilkinson KA,, Coughlan JL,, Weeks KM . 2005. RNA structure analysis at single nucleotide resolution by selective 2′-hydroxyl acylation and primer extension (SHAPE). J Am Chem Soc 127 : 4223– 4231.[PubMed]
186. Flynn RA,, Zhang QC,, Spitale RC,, Lee B,, Mumbach MR,, Chang HY . 2016. Transcriptome-wide interrogation of RNA secondary structure in living cells with icSHAPE. Nat Protoc 11 : 273– 290.[PubMed]
187. Lu Z,, Zhang QC,, Lee B,, Flynn RA,, Smith MA,, Robinson JT,, Davidovich C,, Gooding AR,, Goodrich KJ,, Mattick JS,, Mesirov JP,, Cech TR,, Chang HY . 2016. RNA duplex map in living cells reveals higher-order transcriptome structure. Cell 165 : 1267– 1279.[PubMed]
188. Kertesz M,, Wan Y,, Mazor E,, Rinn JL,, Nutter RC,, Chang HY,, Segal E . 2010. Genome-wide measurement of RNA secondary structure in yeast. Nature 467 : 103– 107.[PubMed]
189. Choi EK,, Ulanowicz KA,, Nguyen YA,, Frandsen JK,, Mitton-Fry RM . 2017. SHAPE analysis of the htrA RNA thermometer from Salmonella enterica. RNA 23 : 1569– 1581.[PubMed]
190. Righetti F,, Nuss AM,, Twittenhoff C,, Beele S,, Urban K,, Will S,, Bernhart SH,, Stadler PF,, Dersch P,, Narberhaus F . 2016. Temperature-responsive in vitro RNA structurome of Yersinia pseudotuberculosis. Proc Natl Acad Sci U S A 113 : 7237– 7242.[PubMed]
191. Steen KA,, Siegfried NA,, Weeks KM . 2011. Selective 2′-hydroxyl acylation analyzed by protection from exoribonuclease (RNase-detected SHAPE) for direct analysis of covalent adducts and of nucleotide flexibility in RNA. Nat Protoc 6 : 1683– 1694.[PubMed]
192. Watters KE,, Abbott TR,, Lucks JB . 2016. Simultaneous characterization of cellular RNA structure and function with in-cell SHAPE-Seq. Nucleic Acids Res 44 : e12.[CrossRef][PubMed]
193. Lu C,, Ding F,, Chowdhury A,, Pradhan V,, Tomsic J,, Holmes WM,, Henkin TM,, Ke A . 2010. SAM recognition and conformational switching mechanism in the Bacillus subtilisyitJ S box/SAM-I riboswitch. J Mol Biol 404 : 803– 818.[PubMed]
194. Watters KE,, Strobel EJ,, Yu AM,, Lis JT,, Lucks JB . 2016. Cotranscriptional folding of a riboswitch at nucleotide resolution. Nat Struct Mol Biol 23 : 1124– 1131.[PubMed]
195. Dar D,, Shamir M,, Mellin JR,, Koutero M,, Stern-Ginossar N,, Cossart P,, Sorek R . 2016. Term-seq reveals abundant ribo-regulation of antibiotics resistance in bacteria. Science 352 : aad9822.[CrossRef][PubMed]
196. Colgan AM,, Cameron AD,, Kröger C . 2017. If it transcribes, we can sequence it: mining the complexities of host-pathogen-environment interactions using RNA-seq. Curr Opin Microbiol 36 : 37– 46.[PubMed]
197. Massé E,, Vanderpool CK,, Gottesman S . 2005. Effect of RyhB small RNA on global iron use in Escherichia coli. J Bacteriol 187 : 6962– 6971.[PubMed]
198. Westermann AJ,, Gorski SA,, Vogel J . 2012. Dual RNA-seq of pathogen and host. Nat Rev Microbiol 10 : 618– 630.[PubMed]
199. Westermann AJ,, Barquist L,, Vogel J . 2017. Resolving host-pathogen interactions by dual RNA-seq. PLoS Pathog 13 : e1006033.[CrossRef][PubMed]
200. Baddal B,, Muzzi A,, Censini S,, Calogero RA,, Torricelli G,, Guidotti S,, Taddei AR,, Covacci A,, Pizza M,, Rappuoli R,, Soriani M,, Pezzicoli A . 2015. Dual RNA-seq of nontypeable Haemophilus influenzae and host cell transcriptomes reveals novel insights into host-pathogen cross talk. mBio 6 : e01765-15.[CrossRef][PubMed]
201. Vanderpool CK,, Gottesman S . 2004. Involvement of a novel transcriptional activator and small RNA in post-transcriptional regulation of the glucose phosphoenolpyruvate phosphotransferase system. Mol Microbiol 54 : 1076– 1089.[PubMed]
202. Barquist L,, Westermann AJ,, Vogel J . 2016. Molecular phenotyping of infection-associated small non-coding RNAs. Philos Trans R Soc Lond B Biol Sci 371 : 20160081.[CrossRef][PubMed]
203. van Opijnen T,, Camilli A . 2013. Transposon insertion sequencing: a new tool for systems-level analysis of microorganisms. Nat Rev Microbiol 11 : 435– 442.[PubMed]
204. Chao MC,, Abel S,, Davis BM,, Waldor MK . 2016. The design and analysis of transposon insertion sequencing experiments. Nat Rev Microbiol 14 : 119– 128.[PubMed]
205. Barquist L,, Boinett CJ,, Cain AK . 2013. Approaches to querying bacterial genomes with transposon-insertion sequencing. RNA Biol 10 : 1161– 1169.[PubMed]
206. Mann B,, van Opijnen T,, Wang J,, Obert C,, Wang YD,, Carter R,, McGoldrick DJ,, Ridout G,, Camilli A,, Tuomanen EI,, Rosch JW . 2012. Control of virulence by small RNAs in Streptococcus pneumoniae. PLoS Pathog 8 : e1002788.[CrossRef][PubMed]
207. Joshi SM,, Pandey AK,, Capite N,, Fortune SM,, Rubin EJ,, Sassetti CM . 2006. Characterization of mycobacterial virulence genes through genetic interaction mapping. Proc Natl Acad Sci U S A 103 : 11760– 11765.[PubMed]
208. Maier L,, Diard M,, Sellin ME,, Chouffane ES,, Trautwein-Weidner K,, Periaswamy B,, Slack E,, Dolowschiak T,, Stecher B,, Loverdo C,, Regoes RR,, Hardt WD . 2014. Granulocytes impose a tight bottleneck upon the gut luminal pathogen population during Salmonella Typhimurium colitis. PLoS Pathog 10 : e1004557.[CrossRef][PubMed]
209. Abel S,, Abel zur Wiesch P,, Chang HH,, Davis BM,, Lipsitch M,, Waldor MK . 2015. Sequence tag-based analysis of microbial population dynamics. Nat Methods 12 : 223– 226.[PubMed]
210. Larson MH,, Gilbert LA,, Wang X,, Lim WA,, Weissman JS,, Qi LS . 2013. CRISPR interference (CRISPRi) for sequence-specific control of gene expression. Nat Protoc 8 : 2180– 2196.[PubMed]
211. Hawkins JS,, Wong S,, Peters JM,, Almeida R,, Qi LS . 2015. Targeted transcriptional repression in bacteria using CRISPR interference (CRISPRi). Methods Mol Biol 1311 : 349– 362.[PubMed]
212. Saliba AE,, C Santos S,, Vogel J . 2017. New RNA-seq approaches for the study of bacterial pathogens. Curr Opin Microbiol 35 : 78– 87.[PubMed]
213. Smirnov A,, Schneider C,, Hör J,, Vogel J . 2017. Discovery of new RNA classes and global RNA-binding proteins. Curr Opin Microbiol 39 : 152– 160.[PubMed]
214. Waters SA,, McAteer SP,, Kudla G,, Pang I,, Deshpande NP,, Amos TG,, Leong KW,, Wilkins MR,, Strugnell R,, Gally DL,, Tollervey D,, Tree JJ . 2017. Small RNA interactome of pathogenic E. coli revealed through crosslinking of RNase E. EMBO J 36 : 374– 387.[PubMed]
215. Melamed S,, Peer A,, Faigenbaum-Romm R,, Gatt YE,, Reiss N,, Bar A,, Altuvia Y,, Argaman L,, Margalit H . 2016. Global mapping of small RNA-target interactions in bacteria. Mol Cell 63 : 884– 897.[PubMed]
216. Lalaouna D,, Carrier MC,, Semsey S,, Brouard JS,, Wang J,, Wade JT,, Masse E . 2015. A 3′ external transcribed spacer in a tRNA transcript acts as a sponge for small RNAs to prevent transcriptional noise. Mol Cell 58 : 393– 405.[PubMed]