1887

Abstract

Gene regulation accomplished by alternative folding of an mRNA is a widely used mechanism. Classical examples are the various transcriptional attenuation mechanisms that employ, for example, leader peptide translation, or binding of a modified protein, an uncharged tRNA or an antisense RNA to the 5′ untranslated region of an mRNA. With the discovery of transcriptional and translational riboswitches, it became clear that small metabolites or even metal ions can also alter RNA secondary structures and, hence, gene expression. In addition, biophysical factors like temperature can affect RNA folding, as exemplified by RNA thermometers. We have investigated in detail the type I toxin–antitoxin system /SR4 from . The antitoxin SR4 is a -encoded regulatory RNA that neutralizes BsrG toxin action. SR4 prevents toxin expression by promoting degradation of the toxin mRNA and inhibiting its translation. In addition, upon temperature shock the amount of toxin mRNA decreases significantly. Here, we demonstrate that heat shock induces a refolding in the central region of the toxin mRNA that makes it more accessible to degradation by RNases Y and J1. Furthermore, we show that BsrG might play a role at the onset of stationary phase, when the antitoxin SR4 can no longer prevent toxin synthesis.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.000247
2016-03-01
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/micro/162/3/590.html?itemId=/content/journal/micro/10.1099/mic.0.000247&mimeType=html&fmt=ahah

References

  1. Brantl S. 2004; Bacterial gene regulation: from transcription attenuation to riboswitches and ribozymes. Trends Microbiol 12:473–475 [View Article][PubMed]
    [Google Scholar]
  2. Brantl S. 2012a; Acting antisense: plasmid- and chromosome-encoded sRNAs from Gram-positive bacteria. Future Microbiol 7:853–871 [View Article][PubMed]
    [Google Scholar]
  3. Brantl S. 2012b; Bacterial type I toxin-antitoxin systems. RNA Biol 9:1488–1490 [View Article][PubMed]
    [Google Scholar]
  4. Brantl S., Brückner R. 2014; Small regulatory RNAs from low-GC Gram-positive bacteria. RNA Biol 11:443–456 [View Article][PubMed]
    [Google Scholar]
  5. Brantl S., Jahn N. 2015; sRNAs in bacterial type I and type III toxin-antitoxin systems. FEMS Microbiol Rev 39:413–427 [View Article][PubMed]
    [Google Scholar]
  6. Brantl S., Wagner E. G. H. 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[PubMed]
    [Google Scholar]
  7. Breaker R. R. 2012; Riboswitches and the RNA world. Cold Spring Harb Perspect Biol 4:a003566 [View Article][PubMed]
    [Google Scholar]
  8. Coppins R. L., Hall K. B., Groisman E. A. 2007; The intricate world of riboswitches. Curr Opin Microbiol 10:176–181 [View Article][PubMed]
    [Google Scholar]
  9. Dambach M. D., Winkler W. C. 2009; Expanding roles for metabolite-sensing regulatory RNAs. Curr Opin Microbiol 12:161–169 [View Article][PubMed]
    [Google Scholar]
  10. Dörr T., Vulić M., Lewis K. 2010; Ciprofloxacin causes persister formation by inducing the TisB toxin in Escherichia coli . PLoS Biol 8:e1000317 [View Article][PubMed]
    [Google Scholar]
  11. Durand S., Jahn N., Condon C., Brantl S. 2012a; Type I toxin-antitoxin systems in Bacillus subtilis . RNA Biol 9:1491–1497 [View Article][PubMed]
    [Google Scholar]
  12. Durand S., Gilet L., Bessières P., Nicolas P., Condon C. 2012b; Three essential ribonucleases—RNase Y, J1, and III—control the abundance of a majority of Bacillus subtilis mRNAs. PLoS Genet 8:e1002520 [View Article][PubMed]
    [Google Scholar]
  13. Even S., Pellegrini O., Zig L., Labas V., Vinh J., Bréchemmier-Baey D., Putzer H. 2005; Ribonucleases J1 and J2: two novel endoribonucleases in B. subtilis with functional homology to E. coli RNase E. Nucleic Acids Res 33:2141–2152 [View Article][PubMed]
    [Google Scholar]
  14. Figaro S., Durand S., Gilet L., Cayet N., Sachse M., Condon C. 2013; Bacillus subtilis mutants with knockouts of the genes encoding ribonucleases RNase Y and RNase J1 are viable, with major defects in cell morphology, sporulation, and competence. J Bacteriol 195:2340–2348 [View Article][PubMed]
    [Google Scholar]
  15. Gerdes K., Wagner E. G. H. 2007; RNA antitoxins. Curr Opin Microbiol 10:117–124 [View Article][PubMed]
    [Google Scholar]
  16. Gimpel M., Heidrich N., Mäder U., Krügel H., Brantl S. 2010; A dual-function sRNA from B. subtilis: SR1 acts as a peptide encoding mRNA on the gapA operon. Mol Microbiol 76:990–1009 [View Article][PubMed]
    [Google Scholar]
  17. Giuliodori A. M., Di Pietro F., Marzi S., Masquida B., Wagner R., Romby P., Gualerzi C. O., Pon C. L. 2010; The cspA mRNA is a thermosensor that modulates translation of the cold-shock protein CspA. Mol Cell 37:21–33 [View Article][PubMed]
    [Google Scholar]
  18. Guo Y., Quiroga C., Chen Q., McAnulty M. J., Benedik M. J., Wood T. K., Wang X. 2014; RalR (a DNase) and RalA (a small RNA) form a type I toxin–antitoxin system in Escherichia coli . Nucleic Acids Res 42:6448–6462 [View Article][PubMed]
    [Google Scholar]
  19. Heidrich N., Brantl S. 2003; Antisense-RNA mediated transcriptional attenuation: importance of a U-turn loop structure in the target RNA of plasmid pIP501 for efficient inhibition by the antisense RNA. J Mol Biol 333:917–929 [View Article][PubMed]
    [Google Scholar]
  20. 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 [View Article][PubMed]
    [Google Scholar]
  21. 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 [View Article][PubMed]
    [Google Scholar]
  22. Jahn N., Brantl S. 2013; One antitoxin—two functions: SR4 controls toxin mRNA decay and translation. Nucleic Acids Res 41:9870–9880 [View Article][PubMed]
    [Google Scholar]
  23. Jahn N., Preis H., Wiedemann C., Brantl S. 2012; BsrG/SR4 from Bacillus subtilis—the first temperature-dependent type I toxin–antitoxin system. Mol Microbiol 83:579–598 [View Article][PubMed]
    [Google Scholar]
  24. Jahn N., Brantl S., Strahl H. 2015; Against the mainstream: the membrane-associated type I toxin BsrG from Bacillus subtilis interferes with cell envelope biosynthesis without increasing membrane permeability. Mol Microbiol 98:651–666 [View Article][PubMed]
    [Google Scholar]
  25. Kawano M. 2012; Divergently overlapping cis-encoded antisense RNA regulating toxin-antitoxin systems from E. coli: hok/sok . ldr/rdl, symE/symR. RNA Biol 9:1520–1527 [View Article][PubMed]
    [Google Scholar]
  26. Kortmann J., Narberhaus F. 2012; Bacterial RNA thermometers: molecular zippers and switches. Nat Rev Microbiol 10:255–265 [View Article][PubMed]
    [Google Scholar]
  27. Laalami S., Bessières P., Rocca A., Zig L., Nicolas P., Putzer H. 2013; Bacillus subtilis RNase Y activity in vivo analysed by tiling microarrays. PLoS One 8:e54062 [View Article][PubMed]
    [Google Scholar]
  28. Laalami S., Zig L., Putzer H. 2014; Initiation of mRNA decay in bacteria. Cell Mol Life Sci 71:1799–1828 [View Article][PubMed]
    [Google Scholar]
  29. 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 [View Article][PubMed]
    [Google Scholar]
  30. Meißner C., Jahn N., Brantl S. 2016; In vitro characterization of the type I toxin-antitoxin system bsrE/SR5 from Bacillus subtilis. J Biol Chem . 291:560–571
    [Google Scholar]
  31. Müller P., Jahn N., Ring C., Maiwald C., Neubert R., Meißner C., Brantl S. 2016; bsrE/SR5 – a multistress responsive type I TA system from B. subtilis . RNA Biol (in press)
    [Google Scholar]
  32. Narberhaus F. 2010; Translational control of bacterial heat shock and virulence genes by temperature-sensing mRNAs. RNA Biol 7:84–89 [View Article][PubMed]
    [Google Scholar]
  33. Narberhaus F., Waldminghaus T., Chowdhury S. 2006; RNA thermometers. FEMS Microbiol Rev 30:3–16 [View Article][PubMed]
    [Google Scholar]
  34. Nechooshtan G., Elgrably-Weiss M., Sheaffer A., Westhof E., Altuvia S. 2009; A pH-responsive riboregulator. Genes Dev 23:2650–2662 [View Article][PubMed]
    [Google Scholar]
  35. Newman J. A., Hewitt L., Rodrigues C., Solovyova A. S., Harwood C. R., Lewis R. J. 2012; Dissection of the network of interactions that links RNA processing with glycolysis in the Bacillus subtilis degradosome. J Mol Biol 416:121–136 [View Article][PubMed]
    [Google Scholar]
  36. Oussenko I. A., Bechhofer D. H. 2000; The yvaJ gene of Bacillus subtilis encodes a 3′-to-5′ exoribonuclease and is not essential in a strain lacking polynucleotide phosphorylase. J Bacteriol 182:2639–2642 [View Article][PubMed]
    [Google Scholar]
  37. Righetti F., Narberhaus F. 2014; How to find RNA thermometers. Front Cell Infect Microbiol 4:132 [View Article][PubMed]
    [Google Scholar]
  38. Roth A., Breaker R. R. 2009; The structural and functional diversity of metabolite-binding riboswitches. Annu Rev Biochem 78:305–334 [View Article][PubMed]
    [Google Scholar]
  39. Shahbabian K., Jamalli A., Zig L., Putzer H. 2009; RNase Y, a novel endoribonuclease, initiates riboswitch turnover in Bacillus subtilis . EMBO J 28:3523–3533 [View Article][PubMed]
    [Google Scholar]
  40. Wagner E. G. H., Unoson C. 2012; The toxin-antitoxin system tisB-istR1: expression, regulation, and biological role in persister phenotypes. RNA Biol 9:1513–1519 [View Article][PubMed]
    [Google Scholar]
  41. Wang W., Bechhofer D. H. 1996; Properties of a Bacillus subtilis polynucleotide phosphorylase deletion strain. J Bacteriol 178:2375–2382[PubMed]
    [Google Scholar]
  42. Weaver K. E. 2012; The par toxin-antitoxin system from Enterococcus faecalis plasmid pAD1 and its chromosomal homologs. RNA Biol 9:1498–1503 [View Article][PubMed]
    [Google Scholar]
  43. Weel-Sneve R., Kristiansen K. I., Odsbu I., Dalhus B., Booth J., Rognes T., Skarstad K., Bjørås M. 2013; Single transmembrane peptide DinQ modulates membrane-dependent activities. PLoS Genet 9:e1003260 [View Article][PubMed]
    [Google Scholar]
  44. Yanofsky C. 2007; RNA-based regulation of genes of tryptophan synthesis and degradation, in bacteria. RNA 13:1141–1154 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.000247
Loading
/content/journal/micro/10.1099/mic.0.000247
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error