Skip to main content
SpringerLink
Log in

An overview of RNAs with regulatory functions in gram-positive bacteria

  • Review
  • Published:
Cellular and Molecular Life Sciences Aims and scope Submit manuscript

Abstract

During the last decade, RNA molecules with regulatory functions on gene expression have benefited from a renewed interest. In bacteria, recent high throughput computational and experimental approaches have led to the discovery that 10–20% of all genes code for RNAs with critical regulatory roles in metabolic, physiological and pathogenic processes. The trans-acting RNAs comprise the noncoding RNAs, RNAs with a short open reading frame and antisense RNAs. Many of these RNAs act through binding to their target mRNAs while others modulate protein activity or target DNA. The cis-acting RNAs include regulatory regions of mRNAs that can respond to various signals. These RNAs often provide the missing link between sensing changing conditions in the environment and fine-tuning the subsequent biological responses. Information on their various functions and modes of action has been well documented for gram-negative bacteria. Here, we summarize the current knowledge of regulatory RNAs in gram-positive bacteria.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  1. Waters LS, Storz G (2009) Regulatory RNAs in bacteria. Cell 136:615–628

    CAS  PubMed  Google Scholar 

  2. Vogel J, Wagner EG (2007) Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol 10:262–270

    CAS  PubMed  Google Scholar 

  3. Gottesman S (2005) Micros for microbes: non-coding regulatory RNAs in bacteria. Trends Genet 21:399–404

    CAS  PubMed  Google Scholar 

  4. Tomizawa J, Itoh T, Selzer G, Som T (1981) Inhibition of ColE1 RNA primer formation by a plasmid-specified small RNA. Proc Natl Acad Sci USA 78:1421–1425

    CAS  PubMed  Google Scholar 

  5. Stougaard P, Molin S, Nordstrom K (1981) RNAs involved in copy-number control and incompatibility of plasmid R1. Proc Natl Acad Sci USA 78:6008–6012

    CAS  PubMed  Google Scholar 

  6. Andersen J, Forst SA, Zhao K, Inouye M, Delihas N (1989) The function of micF RNA micF RNA is a major factor in the thermal regulation of OmpF protein in Escherichia coli. J Biol Chem 264:17961–17970

    CAS  PubMed  Google Scholar 

  7. Delihas N (1997) Antisense micF RNA and 5′-UTR of the target ompF RNA: phylogenetic conservation of primary and secondary structures. Nucleic Acids Symp Ser 36:33–35

    CAS  PubMed  Google Scholar 

  8. Livny J, Teonadi H, Livny M, Waldor MK (2008) High-throughput, kingdom-wide prediction and annotation of bacterial non-coding RNAs. PLoS ONE 3:e3197

    PubMed  Google Scholar 

  9. Marchais A, Naville M, Bohn C, Bouloc P, Gautheret D (2009) Single-pass classification of all noncoding sequences in a bacterial genome using phylogenetic profiles. Genome Res 19:1084–1092

    CAS  PubMed  Google Scholar 

  10. 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

    PubMed  Google Scholar 

  11. Landt SG, Abeliuk E, McGrath PT, Lesley JA, McAdams HH, Shapiro L (2008) Small non-coding RNAs in Caulobacter crescentus. Mol Microbiol 68:600–614

    CAS  PubMed  Google Scholar 

  12. 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, Regnault B, Coppee JY, Lecuit M, Johansson J, Cossart P (2009) The Listeria transcriptional landscape from saprophytism to virulence. Nature 459:950–956

    CAS  PubMed  Google Scholar 

  13. Fozo EM, Hemm MR, Storz G (2008) Small toxic proteins and the antisense RNAs that repress them. Microbiol Mol Biol Rev 72:579–589

    CAS  PubMed  Google Scholar 

  14. Romby P, Vandenesch F, Wagner EG (2006) The role of RNAs in the regulation of virulence-gene expression. Curr Opin Microbiol 9:229–236

    CAS  PubMed  Google Scholar 

  15. Toledo-Arana A, Repoila F, Cossart P (2007) Small noncoding RNAs controlling pathogenesis. Curr Opin Microbiol 10:182–188

    CAS  PubMed  Google Scholar 

  16. Bejerano-Sagie M, Xavier KB (2007) The role of small RNAs in quorum sensing. Curr Opin Microbiol 10:189–198

    CAS  PubMed  Google Scholar 

  17. Vogel J (2009) A rough guide to the non-coding RNA world of Salmonella. Mol Microbiol 71:1–11

    CAS  PubMed  Google Scholar 

  18. Marraffini LA, Sontheimer EJ (2008) CRISPR interference limits horizontal gene transfer in staphylococci by targeting DNA. Science 322:1843–1845

    CAS  PubMed  Google Scholar 

  19. Marraffini LA, Sontheimer EJ (2009) Invasive DNA, Chopped and in the CRISPR. Structure 17:786–788

    CAS  PubMed  Google Scholar 

  20. Babitzke P, Romeo T (2007) CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163

    CAS  PubMed  Google Scholar 

  21. Gorke B, Vogel J (2008) Noncoding RNA control of the making and breaking of sugars. Genes Dev 22:2914–2925

    PubMed  Google Scholar 

  22. Wassarman KM (2007) 6S RNA: a small RNA regulator of transcription. Curr Opin Microbiol 10:164–168

    CAS  PubMed  Google Scholar 

  23. Coppins RL, Hall KB, Groisman EA (2007) The intricate world of riboswitches. Curr Opin Microbiol 10:176–181

    CAS  PubMed  Google Scholar 

  24. Henkin TM (2009) RNA-dependent RNA switches in bacteria. Methods Mol Biol 540:207–214

    CAS  PubMed  Google Scholar 

  25. Pichon C, Felden B (2005) Small RNA genes expressed from Staphylococcus aureus genomic and pathogenicity islands with specific expression among pathogenic strains. Proc Natl Acad Sci USA 102:14249–14254

    CAS  PubMed  Google Scholar 

  26. Valverde C, Haas D (2008) Small RNAs controlled by two-component systems. Adv Exp Med Biol 631:54–79

    PubMed  Google Scholar 

  27. 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

    CAS  PubMed  Google Scholar 

  28. Heidrich N, Chinali A, Gerth U, Brantl S (2006) The small untranslated RNA SR1 from the Bacillus subtilis genome is involved in the regulation of arginine catabolism. Mol Microbiol 62:520–536

    CAS  PubMed  Google Scholar 

  29. 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

    CAS  PubMed  Google Scholar 

  30. Huntzinger E, Boisset S, Saveanu C, Benito Y, Geissmann T, Namane A, Lina G, Etienne J, Ehresmann B, Ehresmann C, Jacquier A, Vandenesch F, Romby P (2005) Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24:824–835

    CAS  PubMed  Google Scholar 

  31. 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

    CAS  PubMed  Google Scholar 

  32. 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

    CAS  PubMed  Google Scholar 

  33. 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

    CAS  PubMed  Google Scholar 

  34. Wagner EG, Altuvia S, Romby P (2002) Antisense RNAs in bacteria and their genetic elements. Adv Genet 46:361–398

    CAS  PubMed  Google Scholar 

  35. Weaver KE (2007) Emerging plasmid-encoded antisense RNA regulated systems. Curr Opin Microbiol 10:110–116

    CAS  PubMed  Google Scholar 

  36. Brantl S (2007) Regulatory mechanisms employed by cis-encoded antisense RNAs. Curr Opin Microbiol 10:102–109

    CAS  PubMed  Google Scholar 

  37. Novick RP, Iordanescu S, Projan SJ, Kornblum J, Edelman I (1989) pT181 plasmid replication is regulated by a countertranscript-driven transcriptional attenuator. Cell 59:395–404

    CAS  PubMed  Google Scholar 

  38. Brantl S, Birch-Hirschfeld E, Behnke D (1993) RepR protein expression on plasmid pIP501 is controlled by an antisense RNA-mediated transcription attenuation mechanism. J Bacteriol 175:4052–4061

    CAS  PubMed  Google Scholar 

  39. Brantl S, Wagner EG (1994) Antisense RNA-mediated transcriptional attenuation occurs faster than stable antisense/target RNA pairing: an in vitro study of plasmid pIP501. EMBO J 13:3599–3607

    CAS  PubMed  Google Scholar 

  40. Kwong SM, Skurray RA, Firth N (2006) Replication control of staphylococcal multiresistance plasmid pSK41: an antisense RNA mediates dual-level regulation of Rep expression. J Bacteriol 188:4404–4412

    CAS  PubMed  Google Scholar 

  41. Greenfield TJ, Ehli E, Kirshenmann T, Franch T, Gerdes K, Weaver KE (2000) The antisense RNA of the par locus of pAD1 regulates the expression of a 33-amino-acid toxic peptide by an unusual mechanism. Mol Microbiol 37:652–660

    CAS  PubMed  Google Scholar 

  42. Greenfield TJ, Weaver KE (2000) Antisense RNA regulation of the pAD1 par post-segregational killing system requires interaction at the 5’ and 3’ ends of the RNAs. Mol Microbiol 37:661–670

    CAS  PubMed  Google Scholar 

  43. Silvaggi JM, Perkins JB, Losick R (2005) Small untranslated RNA antitoxin in Bacillus subtilis. J Bacteriol 187:6641–6650

    CAS  PubMed  Google Scholar 

  44. Mandin P, Repoila F, Vergassola M, Geissmann T, Cossart P (2007) Identification of new noncoding RNAs in Listeria monocytogenes and prediction of mRNA targets. Nucleic Acids Res 35:962–974

    CAS  PubMed  Google Scholar 

  45. Silvaggi JM, Perkins JB, Losick R (2006) Genes for small, noncoding RNAs under sporulation control in Bacillus subtilis. J Bacteriol 188:532–541

    CAS  PubMed  Google Scholar 

  46. Saito S, Kakeshita H, Nakamura K (2009) Novel small RNA-encoding genes in the intergenic regions of Bacillus subtilis. Gene 428:2–8

    CAS  PubMed  Google Scholar 

  47. Novick RP (2003) Autoinduction and signal transduction in the regulation of staphylococcal virulence. Mol Microbiol 48:1429–1449

    CAS  PubMed  Google Scholar 

  48. Novick RP, Geisinger E (2008) Quorum sensing in staphylococci. Annu Rev Genet 42:541–564

    CAS  PubMed  Google Scholar 

  49. Cheung AL, Eberhardt KJ, Chung E, Yeaman MR, Sullam PM, Ramos M, Bayer AS (1994) Diminished virulence of a sar−/agr− mutant of Staphylococcus aureus in the rabbit model of endocarditis. J Clin Invest 94:1815–1822

    CAS  PubMed  Google Scholar 

  50. Gillaspy AF, Hickmon SG, Skinner RA, Thomas JR, Nelson CL, Smeltzer MS (1995) Role of the accessory gene regulator (agr) in pathogenesis of staphylococcal osteomyelitis. Infect Immun 63:3373–3380

    CAS  PubMed  Google Scholar 

  51. Novick RP, Muir TW (1999) Virulence gene regulation by peptides in staphylococci and other Gram-positive bacteria. Curr Opin Microbiol 2:40–45

    CAS  PubMed  Google Scholar 

  52. Benito Y, Kolb FA, Romby P, Lina G, Etienne J, Vandenesch F (2000) Probing the structure of RNAIII, the Staphylococcus aureus agr regulatory RNA, and identification of the RNA domain involved in repression of protein A expression. RNA 6:668–679

    CAS  PubMed  Google Scholar 

  53. Geisinger E, Adhikari RP, Jin R, Ross HF, Novick RP (2006) Inhibition of rot translation by RNAIII, a key feature of agr function. Mol Microbiol 61:1038–1048

    CAS  PubMed  Google Scholar 

  54. Anderson KL, Roberts C, Disz T, Vonstein V, Hwang K, Overbeek R, Olson PD, Projan SJ, Dunman PM (2006) Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J Bacteriol 188:6739–6756

    CAS  PubMed  Google Scholar 

  55. Roberts C, Anderson KL, Murphy E, Projan SJ, Mounts W, Hurlburt B, Smeltzer M, Overbeek R, Disz T, Dunman PM (2006) Characterizing the effect of the Staphylococcus aureus virulence factor regulator, SarA, on log-phase mRNA half-lives. J Bacteriol 188:2593–2603

    CAS  PubMed  Google Scholar 

  56. Livny J, Brencic A, Lory S, Waldor MK (2006) Identification of 17 Pseudomonas aeruginosa sRNAs and prediction of sRNA-encoding genes in 10 diverse pathogens using the bioinformatic tool sRNAPredict2. Nucleic Acids Res 34:3484–3493

    CAS  PubMed  Google Scholar 

  57. Geissmann T, Chevalier C, Cross MJ, Boisset S, Fechter P, Noirot C, Schrenzel J, Francois P, Vandenesch F, Gaspin C, Romby P (2009) A search for small noncoding RNAs in Staphylococcus aureus reveals a conserved motif for regulation. Nucleic Acids Res (in press)

  58. Aiba H (2007) Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10:134–139

    CAS  PubMed  Google Scholar 

  59. Brennan RG, Link TM (2007) Hfq structure, function and ligand binding. Curr Opin Microbiol 10:125–133

    CAS  PubMed  Google Scholar 

  60. Valentin-Hansen P, Eriksen M, Udesen C (2004) The bacterial Sm-like protein Hfq: a key player in RNA transactions. Mol Microbiol 51:1525–1533

    CAS  PubMed  Google Scholar 

  61. Bohn C, Rigoulay C, Bouloc P (2007) No detectable effect of RNA-binding protein Hfq absence in Staphylococcus aureus. BMC Microbiol 7:10

    PubMed  Google Scholar 

  62. Vecerek B, Rajkowitsch L, Sonnleitner E, Schroeder R, Blasi U (2008) The C-terminal domain of Escherichia coli Hfq is required for regulation. Nucleic Acids Res 36:133–143

    CAS  PubMed  Google Scholar 

  63. 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

    CAS  PubMed  Google Scholar 

  64. Christiansen JK, Larsen MH, Ingmer H, Sogaard-Andersen L, Kallipolitis BH (2004) The RNA-binding protein Hfq of Listeria monocytogenes: role in stress tolerance and virulence. J Bacteriol 186:3355–3362

    CAS  PubMed  Google Scholar 

  65. Nielsen JS, Olsen AS, Bonde M, Valentin-Hansen P, Kallipolitis BH (2008) Identification of a sigma B-dependent small noncoding RNA in Listeria monocytogenes. J Bacteriol 190:6264–6270

    CAS  PubMed  Google Scholar 

  66. Trotochaud AE, Wassarman KM (2005) A highly conserved 6S RNA structure is required for regulation of transcription. Nat Struct Mol Biol 12:313–319

    CAS  PubMed  Google Scholar 

  67. 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

    CAS  PubMed  Google Scholar 

  68. Hartmann RK, Gossringer M, Spath B, Fischer S, Marchfelder A (2009) The making of tRNAs and more—RNase P and tRNase Z. Prog Mol Biol Transl Sci 85:319–368

    CAS  PubMed  Google Scholar 

  69. Altman S (2007) A view of RNase P. Mol Biosyst 3:604–607

    CAS  PubMed  Google Scholar 

  70. Marvin MC, Engelke DR (2009) RNase P: increased versatility through protein complexity? RNA Biol 6:40–42

    Article  CAS  PubMed  Google Scholar 

  71. Wegscheid B, Hartmann RK (2007) In vivo and in vitro investigation of bacterial type B RNase P interaction with tRNA 3′-CCA. Nucleic Acids Res 35:2060–2073

    CAS  PubMed  Google Scholar 

  72. Roselli DM, Marsh TL (1990) Purification and characterization of RNase P from Clostridium sporogenes. Mol Microbiol 4:1393–1400

    CAS  PubMed  Google Scholar 

  73. Spitzfaden C, Nicholson N, Jones JJ, Guth S, Lehr R, Prescott CD, Hegg LA, Eggleston DS (2000) The structure of ribonuclease P protein from Staphylococcus aureus reveals a unique binding site for single-stranded RNA. J Mol Biol 295:105–115

    CAS  PubMed  Google Scholar 

  74. Altman S, Wesolowski D, Guerrier-Takada C, Li Y (2005) RNase P cleaves transient structures in some riboswitches. Proc Natl Acad Sci USA 102:11284–11289

    CAS  PubMed  Google Scholar 

  75. Seif E, Altman S (2008) RNase P cleaves the adenine riboswitch and stabilizes pbuE mRNA in Bacillus subtilis. RNA 14:1237–1243

    CAS  PubMed  Google Scholar 

  76. Keenan RJ, Freymann DM, Stroud RM, Walter P (2001) The signal recognition particle. Annu Rev Biochem 70:755–775

    CAS  PubMed  Google Scholar 

  77. Crowley PJ, Svensater G, Snoep JL, Bleiweis AS, Brady LJ (2004) An ffh mutant of Streptococcus mutans is viable and able to physiologically adapt to low pH in continuous culture. FEMS Microbiol Lett 234:315–324

    CAS  PubMed  Google Scholar 

  78. Hasona A, Zuobi-Hasona K, Crowley PJ, Abranches J, Ruelf MA, Bleiweis AS, Brady LJ (2007) Membrane composition changes and physiological adaptation by Streptococcus mutans signal recognition particle pathway mutants. J Bacteriol 189:1219–1230

    CAS  PubMed  Google Scholar 

  79. Hasona A, Crowley PJ, Levesque CM, Mair RW, Cvitkovitch DG, Bleiweis AS, Brady LJ (2005) Streptococcal viability and diminished stress tolerance in mutants lacking the signal recognition particle pathway or YidC2. Proc Natl Acad Sci USA 102:17466–17471

    CAS  PubMed  Google Scholar 

  80. Rosch JW, Vega LA, Beyer JM, Lin A, Caparon MG (2008) The signal recognition particle pathway is required for virulence in Streptococcus pyogenes. Infect Immun 76:2612–2619

    CAS  PubMed  Google Scholar 

  81. Kremer BH, van der Kraan M, Crowley PJ, Hamilton IR, Brady LJ, Bleiweis AS (2001) Characterization of the sat operon in Streptococcus mutans: evidence for a role of Ffh in acid tolerance. J Bacteriol 183:2543–2552

    CAS  PubMed  Google Scholar 

  82. Keiler KC (2008) Biology of trans-translation. Annu Rev Microbiol 62:133–151

    CAS  PubMed  Google Scholar 

  83. Moore SD, Sauer RT (2007) The tmRNA system for translational surveillance and ribosome rescue. Annu Rev Biochem 76:101–124

    CAS  PubMed  Google Scholar 

  84. Saguy M, Gillet R, Metzinger L, Felden B (2005) tmRNA and associated ligands: a puzzling relationship. Biochimie 87:897–903

    CAS  PubMed  Google Scholar 

  85. Abe T, Sakaki K, Fujihara A, Ujiie H, Ushida C, Himeno H, Sato T, Muto A (2008) tmRNA-dependent trans-translation is required for sporulation in Bacillus subtilis. Mol Microbiol 69:1491–1498

    CAS  PubMed  Google Scholar 

  86. Wiegert T, Schumann W (2001) SsrA-mediated tagging in Bacillus subtilis. J Bacteriol 183:3885–3889

    CAS  PubMed  Google Scholar 

  87. Sorek R, Kunin V, Hugenholtz P (2008) CRISPR—a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 6:181–186

    CAS  PubMed  Google Scholar 

  88. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, Romero DA, Horvath P (2007) CRISPR provides acquired resistance against viruses in prokaryotes. Science 315:1709–1712

    CAS  PubMed  Google Scholar 

  89. Brouns SJ, Jore MM, Lundgren M, Westra ER, Slijkhuis RJ, Snijders AP, Dickman MJ, Makarova KS, Koonin EV, van der Oost J (2008) Small CRISPR RNAs guide antiviral defense in prokaryotes. Science 321:960–964

    CAS  PubMed  Google Scholar 

  90. Carte J, Wang R, Li H, Terns RM, Terns MP (2008) Cas6 is an endoribonuclease that generates guide RNAs for invader defense in prokaryotes. Genes Dev 22:3489–3496

    CAS  PubMed  Google Scholar 

  91. Makarova KS, Grishin NV, Shabalina SA, Wolf YI, Koonin EV (2006) A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action. Biol Direct 1:7

    PubMed  Google Scholar 

  92. Barrick JE, Breaker RR (2007) The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol 8:R239

    PubMed  Google Scholar 

  93. Dambach MD, Winkler WC (2009) Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12:161–169

    CAS  PubMed  Google Scholar 

  94. Greenleaf WJ, Frieda KL, Foster DA, Woodside MT, Block SM (2008) Direct observation of hierarchical folding in single riboswitch aptamers. Science 319:630–633

    CAS  PubMed  Google Scholar 

  95. Nudler E, Mironov AS (2004) The riboswitch control of bacterial metabolism. Trends Biochem Sci 29:11–17

    CAS  PubMed  Google Scholar 

  96. Nudler E (2006) Flipping riboswitches. Cell 126:19–22

    CAS  PubMed  Google Scholar 

  97. Soukup JK, Soukup GA (2004) Riboswitches exert genetic control through metabolite-induced conformational change. Curr Opin Struct Biol 14:344–349

    CAS  PubMed  Google Scholar 

  98. Vitreschak AG, Rodionov DA, Mironov AA, Gelfand MS (2004) Riboswitches: the oldest mechanism for the regulation of gene expression? Trends Genet 20:44–50

    CAS  PubMed  Google Scholar 

  99. Serganov A, Patel DJ (2008) Towards deciphering the principles underlying an mRNA recognition code. Curr Opin Struct Biol 18:120–129

    CAS  PubMed  Google Scholar 

  100. Serganov A (2009) The long and the short of riboswitches. Curr Opin Struct Biol 19:251–259

    CAS  PubMed  Google Scholar 

  101. Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, Neph S, Tompa M, Ruzzo WL, Breaker RR (2007) Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35:4809–4819

    CAS  PubMed  Google Scholar 

  102. Winkler WC, Breaker RR (2005) Regulation of bacterial gene expression by riboswitches. Annu Rev Microbiol 59:487–517

    CAS  PubMed  Google Scholar 

  103. Gutierrez-Preciado A, Henkin TM, Grundy FJ, Yanofsky C, Merino E (2009) Biochemical features and functional implications of the RNA-based T-box regulatory mechanism. Microbiol Mol Biol Rev 73:36–61

    CAS  PubMed  Google Scholar 

  104. Vitreschak AG, Mironov AA, Lyubetsky VA, Gelfand MS (2008) Comparative genomic analysis of T-box regulatory systems in bacteria. RNA 14:717–735

    CAS  PubMed  Google Scholar 

  105. Sudarsan N, Hammond MC, Block KF, Welz R, Barrick JE, Roth A, Breaker RR (2006) Tandem riboswitch architectures exhibit complex gene control functions. Science 314:300–304

    CAS  PubMed  Google Scholar 

  106. Roth A, Nahvi A, Lee M, Jona I, Breaker RR (2006) Characteristics of the glmS ribozyme suggest only structural roles for divalent metal ions. RNA 12:607–619

    CAS  PubMed  Google Scholar 

  107. Klein DJ, Ferre-D’Amare AR (2006) Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313:1752–1756

    CAS  PubMed  Google Scholar 

  108. Hampel KJ, Tinsley MM (2006) Evidence for preorganization of the glmS ribozyme ligand binding pocket. Biochemistry 45:7861–7871

    CAS  PubMed  Google Scholar 

  109. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR (2004) Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428:281–286

    CAS  PubMed  Google Scholar 

  110. Brooks KM, Hampel KJ (2009) A rate-limiting conformational step in the catalytic pathway of the glmS ribozyme. Biochemistry 48:5669–5678

    CAS  PubMed  Google Scholar 

  111. Dann CE 3rd, Wakeman CA, Sieling CL, Baker SC, Irnov I, Winkler WC (2007) Structure and mechanism of a metal-sensing regulatory RNA. Cell 130:878–892

    CAS  PubMed  Google Scholar 

  112. Buck J, Furtig B, Noeske J, Wohnert J, Schwalbe H (2007) Time-resolved NMR methods resolving ligand-induced RNA folding at atomic resolution. Proc Natl Acad Sci USA 104:15699–15704

    CAS  PubMed  Google Scholar 

  113. Wickiser JK, Cheah MT, Breaker RR, Crothers DM (2005) The kinetics of ligand binding by an adenine-sensing riboswitch. Biochemistry 44:13404–13414

    CAS  PubMed  Google Scholar 

  114. Morita MT, Tanaka Y, Kodama TS, Kyogoku Y, Yanagi H, Yura T (1999) Translational induction of heat shock transcription factor sigma32: evidence for a built-in RNA thermosensor. Genes Dev 13:655–665

    CAS  PubMed  Google Scholar 

  115. 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

    PubMed  Google Scholar 

  116. Romby P, Springer M (2007) Translational control in biology and medicine. In: Hershey J, Sonenberg N, Matthews M (eds) Cold Spring Harbor Laboratory Press, NY, pp 807–832

  117. Grundy FJ, Henkin TM (1992) Characterization of the Bacillus subtilis rpsD regulatory target site. J Bacteriol 174:6763–6770

    CAS  PubMed  Google Scholar 

  118. Choonee N, Even S, Zig L, Putzer H (2007) Ribosomal protein L20 controls expression of the Bacillus subtilis infC operon via a transcription attenuation mechanism. Nucleic Acids Res 35:1578–1588

    CAS  PubMed  Google Scholar 

  119. Scott LG, Williamson JR (2005) The binding interface between Bacillus stearothermophilus ribosomal protein S15 and its 5′-translational operator mRNA. J Mol Biol 351:280–290

    CAS  PubMed  Google Scholar 

  120. Turnbough CL Jr, Switzer RL (2008) Regulation of pyrimidine biosynthetic gene expression in bacteria: repression without repressors. Microbiol Mol Biol Rev 72:266–300

    CAS  PubMed  Google Scholar 

  121. Merino E, Jensen RA, Yanofsky C (2008) Evolution of bacterial trp operons and their regulation. Curr Opin Microbiol 11:78–86

    CAS  PubMed  Google Scholar 

  122. Yakhnin AV, Yakhnin H, Babitzke P (2008) Function of the Bacillus subtilis transcription elongation factor NusG in hairpin-dependent RNA polymerase pausing in the trp leader. Proc Natl Acad Sci USA 105:16131–16136

    CAS  PubMed  Google Scholar 

  123. Valbuzzi A, Gollnick P, Babitzke P, Yanofsky C (2002) The anti-trp RNA-binding attenuation protein (Anti-TRAP), AT, recognizes the tryptophan-activated RNA binding domain of the TRAP regulatory protein. J Biol Chem 277:10608–10613

    CAS  PubMed  Google Scholar 

  124. Watanabe M, Heddle JG, Kikuchi K, Unzai S, Akashi S, Park SY, Tame JR (2009) The nature of the TRAP–Anti-TRAP complex. Proc Natl Acad Sci USA 106:2176–2181

    CAS  PubMed  Google Scholar 

  125. Cruz-Vera LR, Gong M, Yanofsky C (2008) Physiological effects of anti-TRAP protein activity and tRNA(Trp) charging on trp operon expression in Bacillus subtilis. J Bacteriol 190:1937–1945

    CAS  PubMed  Google Scholar 

  126. Fujita Y (2009) Carbon catabolite control of the metabolic network in Bacillus subtilis. Biosci Biotechnol Biochem 73:245–259

    CAS  PubMed  Google Scholar 

  127. Crutz AM, Steinmetz M, Aymerich S, Richter R, Le Coq D (1990) Induction of levansucrase in Bacillus subtilis: an antitermination mechanism negatively controlled by the phosphotransferase system. J Bacteriol 172:1043–1050

    CAS  PubMed  Google Scholar 

  128. Debarbouille M, Arnaud M, Fouet A, Klier A, Rapoport G (1990) The sacT gene regulating the sacPA operon in Bacillus subtilis shares strong homology with transcriptional antiterminators. J Bacteriol 172:3966–3973

    CAS  PubMed  Google Scholar 

  129. Langbein I, Bachem S, Stulke J (1999) Specific interaction of the RNA-binding domain of the Bacillus subtilis transcriptional antiterminator GlcT with its RNA target, RAT. J Mol Biol 293:795–805

    CAS  PubMed  Google Scholar 

  130. Schilling O, Langbein I, Muller M, Schmalisch MH, Stulke J (2004) A protein-dependent riboswitch controlling ptsGHI operon expression in Bacillus subtilis: RNA structure rather than sequence provides interaction specificity. Nucleic Acids Res 32:2853–2864

    CAS  PubMed  Google Scholar 

  131. Schnetz K, Stulke J, Gertz S, Kruger S, Krieg M, Hecker M, Rak B (1996) LicT, a Bacillus subtilis transcriptional antiterminator protein of the BglG family. J Bacteriol 178:1971–1979

    CAS  PubMed  Google Scholar 

  132. Stulke J, Martin-Verstraete I, Zagorec M, Rose M, Klier A, Rapoport G (1997) Induction of the Bacillus subtilis ptsGHI operon by glucose is controlled by a novel antiterminator, GlcT. Mol Microbiol 25:65–78

    CAS  PubMed  Google Scholar 

  133. Tortosa P, Le Coq D (1995) A ribonucleic antiterminator sequence (RAT) and a distant palindrome are both involved in sucrose induction of the Bacillus subtilis sacXY regulatory operon. Microbiology 141(Pt 11):2921–2927

    CAS  PubMed  Google Scholar 

  134. Lovett PS, Rogers EJ (1996) Ribosome regulation by the nascent peptide. Microbiol Rev 60:366–385

    CAS  PubMed  Google Scholar 

  135. Vazquez-Laslop N, Thum C, Mankin AS (2008) Molecular mechanism of drug-dependent ribosome stalling. Mol Cell 30:190–202

    CAS  PubMed  Google Scholar 

  136. Yao S, Blaustein JB, Bechhofer DH (2008) Erythromycin-induced ribosome stalling and RNase J1-mediated mRNA processing in Bacillus subtilis. Mol Microbiol 69:1439–1449

    CAS  PubMed  Google Scholar 

  137. Sandler P, Weisblum B (1989) Erythromycin-induced ribosome stall in the ermA leader: a barricade to 5′-to-3′ nucleolytic cleavage of the ermA transcript. J Bacteriol 171:6680–6688

    CAS  PubMed  Google Scholar 

  138. Ohtani K, Kawsar HI, Okumura K, Hayashi H, Shimizu T (2003) The VirR/VirS regulatory cascade affects transcription of plasmid-encoded putative virulence genes in Clostridium perfringens strain 13. FEMS Microbiol Lett 222:137–141

    CAS  PubMed  Google Scholar 

  139. 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

    CAS  PubMed  Google Scholar 

  140. Kreikemeyer B, Boyle MD, Buttaro BA, Heinemann M, Podbielski A (2001) Group A streptococcal growth phase-associated virulence factor regulation by a novel operon (Fas) with homologies to two-component-type regulators requires a small RNA molecule. Mol Microbiol 39:392–406

    CAS  PubMed  Google Scholar 

  141. Klenk M, Koczan D, Guthke R, Nakata M, Thiesen HJ, Podbielski A, Kreikemeyer B (2005) Global epithelial cell transcriptional responses reveal Streptococcus pyogenes Fas regulator activity association with bacterial aggressiveness. Cell Microbiol 7:1237–1250

    CAS  PubMed  Google Scholar 

  142. Siller M, Janapatla RP, Pirzada ZA, Hassler C, Zinkl D, Charpentier E (2008) Functional analysis of the group A streptococcal luxS/AI-2 system in metabolism, adaptation to stress and interaction with host cells. BMC Microbiol 8:188

    PubMed  Google Scholar 

  143. Steiner K, Malke H (2001) relA—Independent amino acid starvation response network of Streptococcus pyogenes. J Bacteriol 183:7354–7364

    CAS  PubMed  Google Scholar 

  144. Mangold M, Siller M, Roppenser B, Vlaminckx BJ, Penfound TA, Klein R, Novak R, Novick RP, Charpentier E (2004) Synthesis of group A streptococcal virulence factors is controlled by a regulatory RNA molecule. Mol Microbiol 53:1515–1527

    CAS  PubMed  Google Scholar 

  145. 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(6):1506–1522

    CAS  PubMed  Google Scholar 

  146. Halfmann A, Kovacs M, Hakenbeck R, Bruckner 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

    CAS  PubMed  Google Scholar 

  147. Loh E, Gripenland J, Johansson J (2006) Control of Listeria monocytogenes virulence by 5′-untranslated RNA. Trends Microbiol 14:294–298

    CAS  PubMed  Google Scholar 

  148. Daou-Chabo R, Mathy N, Benard L, Condon C (2009) Ribosomes initiating translation of the hbs mRNA protect it from 5′-to-3′ exoribonucleolytic degradation by RNase J1. Mol Microbiol 71:1538–1550

    CAS  PubMed  Google Scholar 

  149. Condon C (2007) Maturation and degradation of RNA in bacteria. Curr Opin Microbiol 10:271–278

    CAS  PubMed  Google Scholar 

  150. Dreyfus M (2009) Killer and protective ribosomes. Prog Mol Biol Transl Sci 85:423–466

    CAS  PubMed  Google Scholar 

  151. Figueroa-Bossi N, Valentini M, Malleret L, Bossi L (2009) Caught at its own game: regulatory small RNA inactivated by an inducible transcript mimicking its target. Genes Dev 23:000–000

    CAS  Google Scholar 

  152. Overgaard M, Johansen J, Moller-Jensen J, Valentin-Hansen P (2009) Switching off small RNA regulation with trap-mRNA. Mol Microbiol 73:790–800

    CAS  PubMed  Google Scholar 

  153. Navarro L, Jay F, Nomura K, He SY, Voinnet O (2008) Suppression of the microRNA pathway by bacterial effector proteins. Science 321:964–967

    CAS  PubMed  Google Scholar 

  154. Ruiz-Ferrer V, Voinnet O (2009) Roles of plant small RNAs in biotic stress responses. Annu Rev Plant Biol 60:485–510

    CAS  PubMed  Google Scholar 

  155. Brantl S, Wagner EG (2000) Antisense RNA-mediated transcriptional attenuation: an in vitro study of plasmid pT181. Mol Microbiol 35:1469–1482

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are grateful to Brian Jester for critical reading of the manuscript and helpful comments, and we thank members of our teams for stimulating discussions. This work was supported by the European Community FP6 project no. BacRNA-018618 (E.C. and P.R.), the Austrian Science Fund (FWF, project nos. P17238-B09 and W1207-B09) (E.C.), the Austrian Research Promotion Agency (FFG, project no. 812138-SCK/KUG) (E.C.), the Theodor Körner Fonds (E.C.), Umeå University (E.C.), the Swedish Research Council (VR) (E.C.), the CNRS “Centre National de la Recherche Scientifique” (P.R.) and the ANR “Agence Nationale pour la Recherche” (ANR05-MIIM-034-01, ANR09-Blan-436938).

Author information

Authors and Affiliations

  1. Architecture et Réactivité de l’ARN, Université de Strasbourg, CNRS, IBMC, 15 rue René Descartes, 67084, Strasbourg, France

    Pascale Romby

  2. Max F. Perutz Laboratories, University of Vienna, Dr. Bohrgasse 9, 1030, Vienna, Austria

    Emmanuelle Charpentier

  3. The Laboratory for Molecular Infection Medicine Sweden (MIMS), Umeå University, 90187, Umeå, Sweden

    Emmanuelle Charpentier

Authors
  1. Pascale Romby
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emmanuelle Charpentier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Emmanuelle Charpentier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Romby, P., Charpentier, E. An overview of RNAs with regulatory functions in gram-positive bacteria. Cell. Mol. Life Sci. 67, 217–237 (2010). https://doi.org/10.1007/s00018-009-0162-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00018-009-0162-8

Keywords

Search

Navigation