Chapter 26 : Bacterial Small RNAs in Mixed Regulatory Networks

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Regulatory RNAs have emerged as important regulators of gene expression in all kingdoms of life, and many advances toward the understanding of their biology have been achieved in bacteria. Bacterial regulatory RNAs are often also referred to as small RNAs (sRNAs), as most of them range in size from 50 to 400 nucleotides. While it was recognized early on that these sRNAs can ensure extremely diverse biological functions, such as -translation (transfer-messenger RNA), ribonucleolytic activity (RNA moiety of the RNase P), or even involvement in protein secretion (4.5S RNA), the shared efforts of multiple groups in the last 2 decades have led to the identification of a plethora of sRNAs in virtually all bacteria. Many of these act as posttranscriptional regulators of gene expression and generally function by imperfectly base-pairing to target mRNA(s), leading to changes in their translation and/or stability.

Citation: Brosse A, Guillier M. 2019. Bacterial Small RNAs in Mixed Regulatory Networks, p 453-469. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0014-2017
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Figure 1

Examples of connections between transcriptional and posttranscriptional control. Transcriptional regulators/transcriptional regulations and sRNAs/posttranscriptional regulations are in blue and red, respectively. Green nodes indicate nonregulatory target genes. Examples of TR, sRNA, or target found in the depicted circuits are given on the side, and positive or negative regulatory interactions were chosen here based on these examples. Note, however, that all regulations can be positive or negative. Known regulatory interactions between imperfectly base-pairing sRNAs and TRs in and . For clarity, target genes that do not encode regulators are not shown. Unless otherwise indicated, only direct or likely direct interactions are shown. See Table 1 for details.

Citation: Brosse A, Guillier M. 2019. Bacterial Small RNAs in Mixed Regulatory Networks, p 453-469. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0014-2017
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Figure 2

Feedback circuit between the EnvZ-OmpR TCS and OmrA/B sRNAs. OmrA/B sRNAs are transcribed from two adjacent genes and repress expression of multiple mRNAs, including the mRNA, encoding the EnvZ-OmpR TCS. This control decreases the levels of OmpR, but without affecting that of OmpR-P, its phosphorylated form. Because transcription is directly activated by OmpR-P but also responds to the nonphosphorylated OmpR, this feedback circuit allows OmrA/B to indirectly modulate their own synthesis, while expression of other OmpR targets such as or porin genes that are regulated only by OmpR-P remains unchanged. See reference for details.

Citation: Brosse A, Guillier M. 2019. Bacterial Small RNAs in Mixed Regulatory Networks, p 453-469. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0014-2017
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1. Massé E,, Gottesman S . 2002. A small RNA regulates the expression of genes involved in iron metabolism in Escherichia coli. Proc Natl Acad Sci U S A 99 : 4620 4625.[PubMed]
2. Seo SW,, Kim D,, Latif H,, O’Brien EJ,, Szubin R,, Palsson BO . 2014. Deciphering Fur transcriptional regulatory network highlights its complex role beyond iron metabolism in Escherichia coli. Nat Commun 5 : 4910.[CrossRef][PubMed]
3. Salvail H,, Massé E . 2012. Regulating iron storage and metabolism with RNA: an overview of posttranscriptional controls of intracellular iron homeostasis. Wiley Interdiscip Rev RNA 3 : 26 36.[PubMed]
4. Mutalik VK,, Nonaka G,, Ades SE,, Rhodius VA,, Gross CA . 2009. Promoter strength properties of the complete σ E regulon of Escherichia coli and Salmonella enterica. J Bacteriol 191 : 7279 7287.[PubMed]
5. Guo MS,, Updegrove TB,, Gogol EB,, Shabalina SA,, Gross CA,, Storz G . 2014. MicL, a new σ E-dependent sRNA, combats envelope stress by repressing synthesis of Lpp, the major outer membrane lipoprotein. Genes Dev 28 : 1620 1634.[PubMed]
6. Papenfort K,, Pfeiffer V,, Mika F,, Luchhini S,, Hinton JCD,, Vogel J . 2006. σ E-Dependent small RNAs of Salmonella respond to membrane stress by accelerating global omp mRNA decay. Mol Microbiol 62 : 1674 1688.[PubMed]
7. Gogol EB,, Rhodius VA,, Papenfort K,, Vogel J,, Gross CA . 2011. Small RNAs endow a transcriptional activator with essential repressor functions for single-tier control of a global stress regulon. Proc Natl Acad Sci U S A 108 : 12875 12880.[PubMed]
8. Bossi L,, Maloriol D,, Figueroa-Bossi N . 2008. Porin biogenesis activates the σE response in Salmonella hfq mutants. Biochimie 90 : 1539 1544.[PubMed]
9. Chao Y,, Vogel J . 2016. A 3′ UTR-derived small RNA provides the regulatory noncoding arm of the inner membrane stress response. Mol Cell 61 : 352 363.[PubMed]
10. Rhodius VA,, Suh WC,, Nonaka G,, West J,, Gross CA . 2006. Conserved and variable functions of the σ E stress response in related genomes. PLoS Biol 4 : e2.[CrossRef][PubMed]
11. Bury-Moné S,, Nomane Y,, Reymond N,, Barbet R,, Jacquet E,, Imbeaud S,, Jacq A,, Bouloc P . 2009. Global analysis of extracytoplasmic stress signaling in Escherichia coli. PLoS Genet 5 : e1000651.[CrossRef][PubMed]
12. Quereda JJ,, Cossart P . 2017. Regulating bacterial virulence with RNA. Annu Rev Microbiol 71 : 263 280.[PubMed]
13. Caldelari I,, Chao Y,, Romby P,, Vogel J . 2013. RNA-mediated regulation in pathogenic bacteria. Cold Spring Harb Perspect Med 3 : a010298.[CrossRef][PubMed]
14. Majdalani N,, Cunning C,, Sledjeski D,, Elliott T,, Gottesman S . 1998. DsrA RNA regulates translation of RpoS message by an anti-antisense mechanism, independent of its action as an antisilencer of transcription. Proc Natl Acad Sci U S A 95 : 12462 12467.[PubMed]
15. Majdalani N,, Hernandez D,, Gottesman S . 2002. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 46 : 813 826.[PubMed]
16. Mandin P,, Gottesman S . 2010. Integrating anaerobic/aerobic sensing and the general stress response through the ArcZ small RNA. EMBO J 29 : 3094 3107.[PubMed]
17. Zhang A,, Altuvia S,, Tiwari A,, Argaman L,, Hengge-Aronis R,, Storz G . 1998. The OxyS regulatory RNA represses rpoS translation and binds the Hfq (HF-1) protein. EMBO J 17 : 6061 6068.[PubMed]
18. Holmqvist E,, Reimegård J,, Sterk M,, Grantcharova N,, Römling U,, Wagner EG . 2010. Two antisense RNAs target the transcriptional regulator CsgD to inhibit curli synthesis. EMBO J 29 : 1840 1850.[PubMed]
19. Mika F,, Busse S,, Possling A,, Berkholz J,, Tschowri N,, Sommerfeldt N,, Pruteanu M,, Hengge R . 2012. Targeting of csgD by the small regulatory RNA RprA links stationary phase, biofilm formation and cell envelope stress in Escherichia coli. Mol Microbiol 84 : 51 65.[PubMed]
20. Thomason MK,, Fontaine F,, De Lay N,, Storz G . 2012. A small RNA that regulates motility and biofilm formation in response to changes in nutrient availability in Escherichia coli. Mol Microbiol 84 : 17 35.[PubMed]
21. Jørgensen MG,, Nielsen JS,, Boysen A,, Franch T,, Møller-Jensen J,, Valentin-Hansen P . 2012. Small regulatory RNAs control the multi-cellular adhesive lifestyle of Escherichia coli. Mol Microbiol 84 : 36 50.[PubMed]
22. Bordeau V,, Felden B . 2014. Curli synthesis and biofilm formation in enteric bacteria are controlled by a dynamic small RNA module made up of a pseudoknot assisted by an RNA chaperone. Nucleic Acids Res 42 : 4682 4696.[PubMed]
23. De Lay N,, Gottesman S . 2012. A complex network of small non-coding RNAs regulate motility in Escherichia coli. Mol Microbiol 86 : 524 538.[PubMed]
24. Mika F,, Hengge R . 2013. Small regulatory RNAs in the control of motility and biofilm formation in E. coli and Salmonella. Int J Mol Sci 14 : 4560 4579.[PubMed]
25. Jørgensen 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]
26. Bak G,, Lee J,, Suk S,, Kim D,, Young Lee J,, Kim KS,, Choi BS,, Lee Y . 2015. Identification of novel sRNAs involved in biofilm formation, motility, and fimbriae formation in Escherichia coli. Sci Rep 5 : 15287.[CrossRef][PubMed]
27. Parker A,, Cureoglu S,, De Lay N,, Majdalani N,, Gottesman S . 2017. Alternative pathways for Escherichia coli biofilm formation revealed by sRNA overproduction. Mol Microbiol 105 : 309 325.[PubMed]
28. Parker A,, Gottesman S . 2016. Small RNA regulation of TolC, the outer membrane component of bacterial multidrug transporters. J Bacteriol 198 : 1101 1113.[PubMed]
29. Lease RA,, Cusick M,, Belfort M . 1998. Riboregulation in Escherichia coli: DsrA RNA acts by RNA:RNA interactions at multiple loci. Proc Natl Acad Sci U S A 95 : 12456 12461.[PubMed]
30. Lalaouna D,, Morissette A,, Carrier MC,, Massé E . 2015. DsrA regulatory RNA represses both hns and rbsD mRNAs through distinct mechanisms in Escherichia coli. Mol Microbiol 98 : 357 369.[PubMed]
31. Holmqvist E,, Unoson C,, Reimegård J,, Wagner EG . 2012. A mixed double negative feedback loop between the sRNA MicF and the global regulator Lrp. Mol Microbiol 84 : 414 427.[PubMed]
32. Modi SR,, Camacho DM,, Kohanski MA,, Walker GC,, Collins JJ . 2011. Functional characterization of bacterial sRNAs using a network biology approach. Proc Natl Acad Sci U S A 108 : 15522 15527.[PubMed]
33. Sharma CM,, Papenfort K,, Pernitzsch SR,, Mollenkopf HJ,, Hinton JC,, Vogel J . 2011. Pervasive post-transcriptional control of genes involved in amino acid metabolism by the Hfq-dependent GcvB small RNA. Mol Microbiol 81 : 1144 1165.[PubMed]
34. Lee HJ,, Gottesman S . 2016. sRNA roles in regulating transcriptional regulators: Lrp and SoxS regulation by sRNAs. Nucleic Acids Res 44 : 6907 6923.[PubMed]
35. 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]
36. 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]
37. Lenz DH,, Mok KC,, Lilley BN,, Kulkarni RV,, Wingreen NS,, Bassler BL . 2004. The small RNA chaperone Hfq and multiple small RNAs control quorum sensing in Vibrio harveyi and Vibrio cholerae. Cell 118 : 69 82.[PubMed]
38. Tu KC,, Long T,, Svenningsen SL,, Wingreen NS,, Bassler BL . 2010. Negative feedback loops involving small regulatory RNAs precisely control the Vibrio harveyi quorum-sensing response. Mol Cell 37 : 567 579.[PubMed]
39. Hao Y,, Updegrove TB,, Livingston NN,, Storz G . 2016. Protection against deleterious nitrogen compounds: role of σ S-dependent small RNAs encoded adjacent to sdiA. Nucleic Acids Res 44 : 6935 6948.[PubMed]
40. Coornaert A,, Lu A,, Mandin P,, Springer M,, Gottesman S,, Guillier M . 2010. MicA sRNA links the PhoP regulon to cell envelope stress. Mol Microbiol 76 : 467 479.[PubMed]
41. Coornaert A,, Chiaruttini C,, Springer M,, Guillier M . 2013. Post-transcriptional control of the Escherichia coli PhoQ-PhoP two-component system by multiple sRNAs involves a novel pairing region of GcvB. PLoS Genet 9 : e1003156.[CrossRef][PubMed]
42. Wang H,, Yin X,, Wu Orr M,, Dambach M,, Curtis R,, Storz G . 2017. Increasing intracellular magnesium levels with the 31-amino acid MgtS protein. Proc Natl Acad Sci U S A 114 : 5689 5694.[PubMed]
43. Batchelor E,, Goulian M . 2003. Robustness and the cycle of phosphorylation and dephosphorylation in a two-component regulatory system. Proc Natl Acad Sci U S A 100 : 691 696.[PubMed]
44. Brosse A,, Korobeinikova A,, Gottesman S,, Guillier M . 2016. Unexpected properties of sRNA promoters allow feedback control via regulation of a two-component system. Nucleic Acids Res 44 : 9650 9666.
45. DebRoy S,, Gebbie M,, Ramesh A,, Goodson JR,, Cruz MR,, van Hoof A,, Winkler WC,, Garsin DA . 2014. Riboswitches. A riboswitch-containing sRNA controls gene expression by sequestration of a response regulator. Science 345 : 937 940.[PubMed]
46. 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]
47. Shimoni Y,, Friedlander G,, Hetzroni G,, Niv G,, Altuvia S,, Biham O,, Margalit H . 2007. Regulation of gene expression by small non-coding RNAs: a quantitative view. Mol Syst Biol 3 : 138.[CrossRef][PubMed]
48. Hershey JW,, Sonenberg N,, Mathews MB . 2012. Principles of translational control: an overview. Cold Spring Harb Perspect Biol 4 : a011528.[CrossRef][PubMed]
49. Springer M, . 1996. Translational control of gene expression in E. coli and bacteriophage, p 85 126. In Lin EC,, Lynch AS (ed), Regulation of Gene Expression in Escherichia coli. R G Landes Co, Austin, TX.
50. Nomura M,, Gourse R,, Baughman G . 1984. Regulation of the synthesis of ribosomes and ribosomal components. Ann Rev Biochem 53 : 73 117.[PubMed]
51. Levine E,, Hwa T . 2008. Small RNAs establish gene expression thresholds. Curr Opin Microbiol 11 : 574 579.[PubMed]
52. Møller T,, Franch T,, Udesen C,, Gerdes K,, Valentin-Hansen P . 2002. Spot 42 RNA mediates discoordinate expression of the E. coli galactose operon. Genes Dev 16 : 1696 1706.[PubMed]
53. Desnoyers G,, Morissette A,, Prévost K,, Massé E . 2009. Small RNA-induced differential degradation of the polycistronic mRNA iscRSUA. EMBO J 28 : 1551 1561.[PubMed]
54. Massé E,, Escorcia FE,, Gottesman S . 2003. Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli. Genes Dev 17 : 2374 2383.[PubMed]
55. Levine E,, Zhang Z,, Kuhlman T,, Hwa T . 2007. Quantitative characteristics of gene regulation by small RNA. PLoS Biol 5 : e229.[CrossRef][PubMed]
56. Alon U . 2007. Network motifs: theory and experimental approaches. Nat Rev Genet 8 : 450 461.[PubMed]
57. Grantcharova N,, Peters V,, Monteiro C,, Zakikhany K,, Römling U . 2010. Bistable expression of CsgD in biofilm development of Salmonella enterica serovar Typhimurium. J Bacteriol 192 : 456 466.[PubMed]
58. Gottesman S,, Storz G . 2011. Bacterial small RNA regulators: versatile roles and rapidly evolving variations. Cold Spring Harb Perspect Biol 3 : a003798.[CrossRef][PubMed]
59. Peer A,, Margalit H . 2014. Evolutionary patterns of Escherichia coli small RNAs and their regulatory interactions. RNA 20 : 994 1003.[PubMed]
60. Figueroa-Bossi N,, Valentini M,, Malleret L,, Fiorini F,, Bossi L . 2009. Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes Dev 23 : 2004 2015.[PubMed]
61. Lalaouna D,, Carrier MC,, Semsey S,, Brouard JS,, Wang J,, Wade JT,, Massé 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]
62. Miyakoshi M,, Chao Y,, Vogel J . 2015. Cross talk between ABC transporter mRNAs via a target mRNA-derived sponge of the GcvB small RNA. EMBO J 34 : 1478 1492.[PubMed]
63. Bossi L,, Figueroa-Bossi N . 2016. Competing endogenous RNAs: a target-centric view of small RNA regulation in bacteria. Nat Rev Microbiol 14 : 775 784.[PubMed]
64. Fender A,, Elf J,, Hampel K,, Zimmermann B,, Wagner EG . 2010. RNAs actively cycle on the Sm-like protein Hfq. Genes Dev 24 : 2621 2626.[PubMed]
65. Moon K,, Gottesman S . 2011. Competition among Hfq-binding small RNAs in Escherichia coli. Mol Microbiol 82 : 1545 1562.[PubMed]
66. Hussein R,, Lim HN . 2011. Disruption of small RNA signaling caused by competition for Hfq. Proc Natl Acad Sci U S A 108 : 1110 1115.[PubMed]
67. Beisel CL,, Storz G . 2010. Base pairing small RNAs and their roles in global regulatory networks. FEMS Microbiol Rev 34 : 866 882.[PubMed]
68. Nitzan M,, Rehani R,, Margalit H . 2017. Integration of bacterial small RNAs in regulatory networks. Annu Rev Biophys 46 : 131 148.[PubMed]
69. Tu KC,, Waters CM,, Svenningsen SL,, Bassler BL . 2008. A small-RNA-mediated negative feedback loop controls quorum-sensing dynamics in Vibrio harveyi. Mol Microbiol 70 : 896 907.[PubMed]
70. Svenningsen SL,, Waters CM,, Bassler BL . 2008. A negative feedback loop involving small RNAs accelerates Vibrio cholerae’s transition out of quorum-sensing mode. Genes Dev 22 : 226 238.[PubMed]
71. 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]
72. Beisel CL,, Storz G . 2011. The base-pairing RNA Spot 42 participates in a multioutput feedforward loop to help enact catabolite repression in Escherichia coli. Mol Cell 41 : 286 297.[PubMed]
73. Papenfort K,, Espinosa E,, Casadesús J,, Vogel J . 2015. Small RNA-based feedforward loop with AND-gate logic regulates extrachromosomal DNA transfer in Salmonella. Proc Natl Acad Sci U S A 112 : E4772 4781.[PubMed]
74. Mandin P,, Gottesman S . 2009. A genetic approach for finding small RNAs regulators of genes of interest identifies RybC as regulating the DpiA/DpiB two-component system. Mol Microbiol 72 : 551 565.[PubMed]
75. De Lay N,, Gottesman S . 2009. The Crp-activated small noncoding regulatory RNA CyaR (RyeE) links nutritional status to group behavior. J Bacteriol 191 : 461 476.[PubMed]
76. Vogt SL,, Evans AD,, Guest RL,, Raivio TL . 2014. The Cpx envelope stress response regulates and is regulated by small noncoding RNAs. J Bacteriol 196 : 4229 4238.[PubMed]
77. Johansen J,, Eriksen M,, Kallipolitis B,, Valentin-Hansen P . 2008. Down-regulation of outer membrane proteins by noncoding RNAs: unraveling the cAMP-CRP- and σ E-dependent CyaR- ompX regulatory case. J Mol Biol 383 : 1 9.[PubMed]
78. 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]
79. Durand S,, Storz G . 2010. Reprogramming of anaerobic metabolism by the FnrS small RNA. Mol Microbiol 75 : 1215 1231.[PubMed]
80. Opdyke JA,, Kang JG,, Storz G . 2004. GadY, a small-RNA regulator of acid response genes in Escherichia coli. J Bacteriol 186 : 6698 6705.[PubMed]
81. Urbanowski ML,, Stauffer LT,, Stauffer GV . 2000. The gcvB gene encodes a small untranslated RNA involved in expression of the dipeptide and oligopeptide transport systems in Escherichia coli. Mol Microbiol 37 : 856 868.[PubMed]
82. Reichenbach B,, Gopel Y,, Gorke B . 2009. Dual control by perfectly overlapping σ54- and σ70-promoters adjusts small RNA GlmY expression to different environmental signals. Mol Microbiol 74 : 1054 1070.[PubMed]
83. Gopel Y,, Luttmann D,, Heroven AK,, Reichenbach B,, Dersch P,, Gorke B . 2011. Common and divergent features in transcriptional control of the homologous small RNAs GlmY and GlmZ in Enterobacteriaceae. Nucleic Acids Res 39 : 1294 1309.[PubMed]
84. 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]
85. Moon K,, Gottesman S . 2009. A PhoQ/P-regulated small RNA regulates sensitivity of Escherichia coli to antimicrobial peptides. Mol Microbiol 74 : 1314 1330.[PubMed]
86. Udekwu KI,, Wagner EG . 2007. Sigma E controls biogenesis of the antisense RNA MicA. Nucleic Acids Res 35 : 1279 1288.[PubMed]
87. Johansen J,, Rasmussen AA,, Overgaard M,, Valentin-Hansen P . 2006. Conserved small non-coding RNAs that belong to the σ E regulon: role in down-regulation of outer membrane proteins. J Mol Biol 364 : 1 8.[PubMed]
88. Figueroa-Bossi N,, Lemire S,, Maloriol D,, Balbontin R,, Casadesús J,, Bossi L . 2006. Loss of Hfq activates the σ E-dependent envelope stress response in Salmonella enterica. Mol Microbiol 62 : 838 852.[PubMed]
89. Delihas N,, Forst S . 2001. MicF: an antisense RNA gene involved in response of Escherichia coli to global stress factors. J Mol Biol 313 : 1 12.[PubMed]
90. Corcoran CP,, Podkaminski D,, Papenfort K,, Urban JH,, Hinton JC,, Vogel J . 2012. Superfolder GFP reporters validate diverse new mRNA targets of the classic porin regulator, MicF RNA. Mol Microbiol 84 : 428 445.[PubMed]
91. Peano C,, Wolf J,, Demol J,, Rossi E,, Petiti L,, De Bellis G,, Geiselmann J,, Egli T,, Lacour S,, Landini P . 2015. Characterization of the Escherichia coli σ S core regulon by Chromatin Immunoprecipitation-sequencing (ChIP-seq) analysis. Sci Rep 5 : 10469.[CrossRef][PubMed]
92. Lévi-Meyrueis C,, Monteil V,, Sismeiro O,, Dillies MA,, Monot M,, Jagla B,, Coppée JY,, Dupuy B,, Norel F . 2014. Expanding the RpoS/σ S-network by RNA sequencing and identification of σ S-controlled small RNAs in Salmonella. PLoS One 9 : e96918.[CrossRef][PubMed]
93. Guillier M,, Gottesman S . 2008. The 5′ end of two redundant sRNAs is involved in the regulation of multiple targets, including their own regulator. Nucleic Acids Res 36 : 6781 6794.[PubMed]
94. Altuvia S,, Weinstein-Fischer D,, Zhang A,, Postow L,, Storz G . 1997. A small stable RNA induced by oxidative stress: role as a pleiotropic regulator and antimutator. Cell 90 : 43 53.
95. Altuvia S,, Zhang A,, Argaman L,, Tiwari A,, Storz G . 1998. The Escherichia coli OxyS regulatory RNA represses fhlA translation by blocking ribosome binding. EMBO J 17 : 6069 6075.[PubMed]
96. 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]
97. Thompson KM,, Rhodius VA,, Gottesman S . 2007. σ E regulates and is regulated by a small RNA in Escherichia coli. J Bacteriol 189 : 4243 4256.[PubMed]
98. 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]
99. Vecerek B,, Moll I,, Bläsi U . 2007. Control of Fur synthesis by the non-coding RNA RyhB and iron-responsive decoding. EMBO J 26 : 965 975.[PubMed]
100. Fröhlich KS,, Papenfort K,, Berger AA,, Vogel J . 2012. A conserved RpoS-dependent small RNA controls the synthesis of major porin OmpD. Nucleic Acids Res 40 : 3623 3640.[PubMed]
101. Vanderpool CK,, Gottesman S . 2007. The novel transcription factor SgrR coordinates the response to glucose-phosphate stress. J Bacteriol 189 : 2238 2248.[PubMed]
102. Polayes DA,, Rice PW,, Garner MM,, Dahlberg JE . 1988. Cyclic AMP-cyclic AMP receptor protein as a repressor of transcription of the spf gene of Escherichia coli. J Bacteriol 170 : 3110 3114.[PubMed]
103. Silva IJ,, Ortega AD,, Viegas SC,, García-Del Portillo F,, Arraiano CM . 2013. An RpoS-dependent sRNA regulates the expression of a chaperone involved in protein folding. RNA 19 : 1253 1265.[PubMed]
104. 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]
105. 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]
106. 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]
107. 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]
108. 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]
109. 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]
110. 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]
111. Yamamoto S,, Mitobe J,, Ishikawa T,, Wai SN,, Ohnishi M,, Watanabe H,, Izumiya H . 2014. Regulation of natural competence by the orphan two-component system sensor kinase ChiS involves a non-canonical transmembrane regulator in Vibrio cholerae. Mol Microbiol 91 : 326 347.[PubMed]
112. Dalia AB,, Lazinski DW,, Camilli A . 2014. Identification of a membrane-bound transcriptional regulator that links chitin and natural competence in Vibrio cholerae. mBio 5 : e01028-13.[CrossRef][PubMed]
113. Yamamoto S,, Izumiya H,, Mitobe J,, Morita M,, Arakawa E,, Ohnishi M,, Watanabe H . 2011. Identification of a chitin-induced small RNA that regulates translation of the tfoX gene, encoding a positive regulator of natural competence in Vibrio cholerae. J Bacteriol 193 : 1953 1965.[PubMed]
114. Sonnleitner E,, Gonzalez N,, Sorger-Domenigg T,, Heeb S,, Richter AS,, Backofen R,, Williams P,, Hüttenhofer A,, Haas D,, Bläsi U . 2011. The small RNA PhrS stimulates synthesis of the Pseudomonas aeruginosa quinolone signal. Mol Microbiol 80 : 868 885.[PubMed]
115. Wilderman PJ,, Sowa NA,, FitzGerald DJ,, FitzGerald PC,, Gottesman S,, Ochsner UA,, Vasil ML . 2004. Identification of tandem duplicate regulatory small RNAs in Pseudomonas aeruginosa involved in iron homeostasis. Proc Natl Acad Sci U S A 101 : 9792 9797.[PubMed]
116. Sonnleitner E,, Haas D . 2011. Small RNAs as regulators of primary and secondary metabolism in Pseudomonas species. Appl Microbiol Biotechnol 91 : 63 79.[PubMed]
117. Wenner N,, Maes A,, Cotado-Sampayo M,, Lapouge K . 2014. NrsZ: a novel, processed, nitrogen-dependent, small non-coding RNA that regulates Pseudomonas aeruginosa PAO1 virulence. Environ Microbiol 16 : 1053 1068.[PubMed]
118. Zhang YF,, Han K,, Chandler CE,, Tjaden B,, Ernst RK,, Lory S . 2017. Probing the sRNA regulatory landscape of P. aeruginosa: post-transcriptional control of determinants of pathogenicity and antibiotic susceptibility. Mol Microbiol 106 : 919 937.[PubMed]
119. 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]
120. Mank NN,, Berghoff BA,, Hermanns YN,, Klug G . 2012. Regulation of bacterial photosynthesis genes by the small noncoding RNA PcrZ. Proc Natl Acad Sci U S A 109 : 16306 16311.[PubMed]
121. Janzon L,, Löfdahl S,, Arvidson S . 1989. Identification and nucleotide sequence of the delta-lysin gene, hld, adjacent to the accessory gene regulator ( agr) of Staphylococcus aureus. Mol Gen Genet 219 : 480 485.[PubMed]
122. Novick RP,, Ross HF,, Projan SJ,, Kornblum J,, Kreiswirth B,, Moghazeh S . 1993. Synthesis of staphylococcal virulence factors is controlled by a regulatory RNA molecule. EMBO J 12 : 3967 3975.[PubMed]
123. 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]
124. Gupta RK,, Luong TT,, Lee CY . 2015. RNAIII of the Staphylococcus aureus agr system activates global regulator MgrA by stabilizing mRNA. Proc Natl Acad Sci U S A 112 : 14036 14041.[PubMed]
125. Xue T,, Zhang X,, Sun H,, Sun B . 2014. ArtR, a novel sRNA of Staphylococcus aureus, regulates α-toxin expression by targeting the 5′ UTR of sarT mRNA. Med Microbiol Immunol 203 : 1 12.[PubMed]
126. Durand S,, Braun F,, Lioliou E,, Romilly C,, Helfer AC,, Kuhn L,, Quittot N,, Nicolas P,, Romby P,, Condon C . 2015. A nitric oxide regulated small RNA controls expression of genes involved in redox homeostasis in Bacillus subtilis. PLoS Genet 11 : e1004957.[CrossRef][PubMed]
127. Durand S,, Braun F,, Helfer AC,, Romby P,, Condon C . 2017. sRNA-mediated activation of gene expression by inhibition of 5′-3′ exonucleolytic mRNA degradation. eLife 6 : e23602.[CrossRef][PubMed]
128. Geissmann T,, Chevalier C,, Cros MJ,, Boisset S,, Fechter P,, Noirot C,, Schrenzel J,, François P,, Vandenesch F,, Gaspin C,, Romby P . 2009. A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved sequence motif for regulation. Nucleic Acids Res 37 : 7239 7257.[PubMed]
129. 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]
130. Nielsen JS,, Christiansen MH,, Bonde M,, Gottschalk S,, Frees D,, Thomsen LE,, Kallipolitis BH . 2011. Searching for small σB-regulated genes in Staphylococcus aureus. Arch Microbiol 193 : 23 34.[PubMed]
131. Kaito C,, Saito Y,, Ikuo M,, Omae Y,, Mao H,, Nagano G,, Fujiyuki T,, Numata S,, Han X,, Obata K,, Hasegawa S,, Yamaguchi H,, Inokuchi K,, Ito T,, Hiramatsu K,, Sekimizu K . 2013. Mobile genetic element SCC mec-encoded psm-mec RNA suppresses translation of agrA and attenuates MRSA virulence. PLoS Pathog 9 : e1003269.[CrossRef][PubMed]
132. Mauro T,, Rouillon A,, Felden B . 2016. Insights into the regulation of small RNA expression: SarA represses the expression of two sRNAs in Staphylococcus aureus. Nucleic Acids Res 44 : 10186 10200.
133. Gaballa A,, Antelmann H,, Aguilar C,, Khakh SK,, Song KB,, Smaldone GT,, Helmann JD . 2008. The Bacillus subtilis iron-sparing response is mediated by a Fur-regulated small RNA and three small, basic proteins. Proc Natl Acad Sci U S A 105 : 11927 11932.[PubMed]
134. Licht A,, Preis S,, Brantl S . 2005. Implication of CcpN in the regulation of a novel untranslated RNA (SR1) in Bacillus subtilis. Mol Microbiol 58 : 189 206.[PubMed]
135. Heidrich N,, Moll I,, Brantl S . 2007. In vitro analysis of the interaction between the small RNA SR1 and its primary target ahrC mRNA. Nucleic Acids Res 35 : 4331 4346.[PubMed]
136. Schmalisch M,, Maiques E,, Nikolov L,, Camp AH,, Chevreux B,, Muffler A,, Rodriguez S,, Perkins J,, Losick R . 2010. Small genes under sporulation control in the Bacillus subtilis genome. J Bacteriol 192 : 5402 5412.[PubMed]
137. Mars RA,, Nicolas P,, Ciccolini M,, Reilman E,, Reder A,, Schaffer M,, Mader U,, Völker U,, van Dijl JM,, Denham EL . 2015. Small regulatory RNA-induced growth rate heterogeneity of Bacillus subtilis. PLoS Genet 11 : e1005046.[CrossRef][PubMed]
138. Marchais A,, Duperrier S,, Durand S,, Gautheret D,, Stragier P . 2011. CsfG, a sporulation-specific, small non-coding RNA highly conserved in endospore formers. RNA Biol 8 : 358 364.[PubMed]
139. Sievers S,, Sternkopf Lillebaek EM,, Jacobsen K,, Lund A,, Mollerup MS,, Nielsen PK,, Kallipolitis BH . 2014. A multicopy sRNA of Listeria monocytogenes regulates expression of the virulence adhesin LapB. Nucleic Acids Res 42 : 9383 9398.[PubMed]
140. Mollerup MS,, Ross JA,, Helfer AC,, Meistrup K,, Romby P,, Kallipolitis BH . 2016. Two novel members of the LhrC family of small RNAs in Listeria monocytogenes with overlapping regulatory functions but distinctive expression profiles. RNA Biol 13 : 895 915.[PubMed]
141. 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]
142. Pappesch R,, Warnke P,, Mikkat S,, Normann J,, Wisniewska-Kucper A,, Huschka F,, Wittmann M,, Khani A,, Schwengers O,, Oehmcke-Hecht S,, Hain T,, Kreikemeyer B,, Patenge N . 2017. The regulatory small RNA MarS supports virulence of Streptococcus pyogenes. Sci Rep 7 : 12241.[CrossRef][PubMed]
143. Acebo P,, Martin-Galiano AJ,, Navarro S,, Zaballos A,, Amblar M . 2012. Identification of 88 regulatory small RNAs in the TIGR4 strain of the human pathogen Streptococcus pneumoniae. RNA 18 : 530 546.[PubMed]
144. Halfmann A,, Kovács M,, Hakenbeck R,, Brückner R . 2007. Identification of the genes directly controlled by the response regulator CiaR in Streptococcus pneumoniae: five out of 15 promoters drive expression of small non-coding RNAs. Mol Microbiol 66 : 110 126.[PubMed]
145. Shimizu T,, Yaguchi H,, Ohtani K,, Banu S,, Hayashi H . 2002. Clostridial VirR/VirS regulon involves a regulatory RNA molecule for expression of toxins. Mol Microbiol 43 : 257 265.[PubMed]


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Table 1

Examples of imperfectly base-pairing small RNAs regulated by and/or regulating TRs in and

Citation: Brosse A, Guillier M. 2019. Bacterial Small RNAs in Mixed Regulatory Networks, p 453-469. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0014-2017
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Table 2

Examples of connections between imperfectly base-pairing sRNAs and TRs in species other than or

Citation: Brosse A, Guillier M. 2019. Bacterial Small RNAs in Mixed Regulatory Networks, p 453-469. In Storz G, Papenfort K (ed), Regulating with RNA in Bacteria and Archaea. ASM Press, Washington, DC. doi: 10.1128/microbiolspec.RWR-0014-2017

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