1887

Abstract

Transcriptional regulation of primary and secondary metabolism is well-studied in , a model organism for antibiotic production and cell differentiation. In contrast, little is known about post-transcriptional regulation and the potential functions of small non-coding RNAs (sRNAs) in this Gram-positive, GC-rich soil bacterium. Here, we report the identification and characterization of scr5239, an sRNA highly conserved in the genus . The sRNA is 159 nt long, composed of five stem–loops, and encoded in the intergenic region between SCO5238 and SCO5239. scr5239 expression is constitutive under several stress and growth conditions but dependent on the nitrogen supply. scr5239 decreases the production of the antibiotic actinorhodin, and represses expression of the extracellular agarase at the post-transcriptional level by direct base pairing to the coding region 33 nt downstream of the ribosome-binding site.

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2012-02-01
2022-01-21
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References

  1. Afonyushkin T., Moll I., Bläsi U., Kaberdin V. R. ( 2003). Temperature-dependent stability and translation of Escherichia coli ompA mRNA. Biochem Biophys Res Commun 311:604–609 [View Article][PubMed]
    [Google Scholar]
  2. Aiba H. ( 2007). Mechanism of RNA silencing by Hfq-binding small RNAs. Curr Opin Microbiol 10:134–139 [View Article][PubMed]
    [Google Scholar]
  3. Argaman L., Hershberg R., Vogel J., Bejerano G., Wagner E. G. H., Margalit H., Altuvia S. ( 2001). Novel small RNA-encoding genes in the intergenic regions of Escherichia coli . Curr Biol 11:941–950 [View Article][PubMed]
    [Google Scholar]
  4. Babitzke P., Romeo T. ( 2007). CsrB sRNA family: sequestration of RNA-binding regulatory proteins. Curr Opin Microbiol 10:156–163 [View Article][PubMed]
    [Google Scholar]
  5. Bentley S. D., Chater K. F., Cerdeño-Tárraga A.-M., Challis G. L., Thomson N. R., James K. D., Harris D. E., Quail M. A., Kieser H. & other authors ( 2002). Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147 [View Article][PubMed]
    [Google Scholar]
  6. Binnie C., Jenish D., Cossar D., Szabo A., Trudeau D., Krygsman P., Malek L. T., Stewart D. I. ( 1997). Expression and characterization of soluble human erythropoietin receptor made in Streptomyces lividans 66. Protein Expr Purif 11:271–278 [View Article][PubMed]
    [Google Scholar]
  7. Bouvier M., Sharma C. M., Mika F., Nierhaus K. H., Vogel J. ( 2008). Small RNA binding to 5′ mRNA coding region inhibits translational initiation. Mol Cell 32:827–837 [View Article][PubMed]
    [Google Scholar]
  8. Brawner M. E., Auerbach J. I., Fornwald J. A., Rosenberg M., Taylor D. P. ( 1985). Characterization of Streptomyces promoter sequences using the Escherichia coli galactokinase gene. Gene 40:191–201 [View Article][PubMed]
    [Google Scholar]
  9. Brockmann H., Pini H., Plotho O. V. ( 1950). Über Actinomycetenfarbstoffe, I. Mitteil.: Actinorhodin, ein roter, antibiotisch wirksamer Farbstoff aus Actinomyceten. Chem Ber 83:161–167 [View Article]
    [Google Scholar]
  10. Buttner M. J., Smith A. M., Bibb M. J. ( 1988). At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2). Cell 52:599–607 [View Article][PubMed]
    [Google Scholar]
  11. Chater K. F. ( 2001). Regulation of sporulation in Streptomyces coelicolor A3(2): a checkpoint multiplex?. Curr Opin Microbiol 4:667–673 [View Article][PubMed]
    [Google Scholar]
  12. Chevalier C., Geissmann T., Helfer A.-C., Romby P. ( 2009). Probing mRNA structure and sRNA–mRNA interactions in bacteria using enzymes and lead(II). Methods Mol Biol 540:215–232
    [Google Scholar]
  13. Claessen D., de Jong W., Dijkhuizen L., Wösten H. A. B. ( 2006). Regulation of Streptomyces development: reach for the sky!. Trends Microbiol 14:313–319 [View Article][PubMed]
    [Google Scholar]
  14. D’Alia D., Nieselt K., Steigele S., Müller J., Verburg I., Takano E. ( 2010). Noncoding RNA of glutamine synthetase I modulates antibiotic production in Streptomyces coelicolor A3(2). J Bacteriol 192:1160–1164 [View Article][PubMed]
    [Google Scholar]
  15. Darfeuille F., Unoson C., Vogel J., Wagner E. G. H. ( 2007). An antisense RNA inhibits translation by competing with standby ribosomes. Mol Cell 26:381–392 [View Article][PubMed]
    [Google Scholar]
  16. Dühring U., Axmann I. M., Hess W. R., Wilde A. ( 2006). An internal antisense RNA regulates expression of the photosynthesis gene isiA . Proc Natl Acad Sci U S A 103:7054–7058 [View Article][PubMed]
    [Google Scholar]
  17. Fröhlich K. S., Vogel J. ( 2009). Activation of gene expression by small RNA. Curr Opin Microbiol 12:674–682 [View Article][PubMed]
    [Google Scholar]
  18. Gaballa A., Antelmann H., Aguilar C., Khakh S. K., Song K.-B., Smaldone G. T., Helmann J. D. ( 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 [View Article][PubMed]
    [Google Scholar]
  19. Gottesman S. ( 2004). The small RNA regulators of Escherichia coli: roles and mechanisms. Annu Rev Microbiol 58:303–328 [View Article][PubMed]
    [Google Scholar]
  20. Gottesman S., McCullen C. A., Guillier M., Vanderpool C. K., Majdalani N., Benhammou J., Thompson K. M., FitzGerald P. C., Sowa N. A., FitzGerald D. J. ( 2006). Small RNA regulators and the bacterial response to stress. Cold Spring Harb Symp Quant Biol 71:1–11 [View Article][PubMed]
    [Google Scholar]
  21. Gruber A. R., Lorenz R., Bernhart S. H., Neuböck R., Hofacker I. L. ( 2008). The Vienna RNA websuite. Nucleic Acids Res 36:Web Server issueW70–W74 [View Article][PubMed]
    [Google Scholar]
  22. 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]
  23. Hodgson D. A. ( 2000). Primary metabolism and its control in streptomycetes: a most unusual group of bacteria. Adv Microb Physiol 42:47–238 [View Article][PubMed]
    [Google Scholar]
  24. Hodgson D. A., Chater K. F. ( 1981). A chromosomal locus controlling extracellular agarase. J Gen Microbiol 124:339–348
    [Google Scholar]
  25. Hopwood D. A., Chater K. F., Dowding J. E., Vivian A. ( 1973). Advances in Streptomyces coelicolor genetics. Bacteriol Rev 37:371–405[PubMed]
    [Google Scholar]
  26. Huntzinger E., Boisset S., Saveanu C., Benito Y., Geissmann T., Namane A., Lina G., Etienne J., Ehresmann B. & other authors ( 2005). Staphylococcus aureus RNAIII and the endoribonuclease III coordinately regulate spa gene expression. EMBO J 24:824–835 [View Article][PubMed]
    [Google Scholar]
  27. Kieser T., Hopwood D. A., Chater K. F., Buttner M. J., Bibb M. J. ( 2000). Practical Streptomyces Genetics Norwich, UK: John Innes Centre;
    [Google Scholar]
  28. Labes G., Bibb M. J., Wohlleben W. ( 1997). Isolation and characterization of a strong promoter element from the Streptomyces ghanaensis phage I19 using the gentamicin resistance gene (aacC1) of Tn1696 as reporter. Microbiology 143:1503–1512 [View Article][PubMed]
    [Google Scholar]
  29. Li H., Jacques P.-E., Ghinet M. G., Brzezinski R., Morosoli R. ( 2005). Determining the functionality of putative Tat-dependent signal peptides in Streptomyces coelicolor A3(2) by using two different reporter proteins. Microbiology 151:2189–2198 [View Article][PubMed]
    [Google Scholar]
  30. Massé E., Escorcia F. E., Gottesman S. ( 2003). Coupled degradation of a small regulatory RNA and its mRNA targets in Escherichia coli . Genes Dev 17:2374–2383 [View Article][PubMed]
    [Google Scholar]
  31. Mattatall N. R., Sanderson K. E. ( 1996). Salmonella typhimurium LT2 possesses three distinct 23S rRNA intervening sequences. J Bacteriol 178:2272–2278[PubMed]
    [Google Scholar]
  32. McAdams H. H., Srinivasan B., Arkin A. P. ( 2004). The evolution of genetic regulatory systems in bacteria. Nat Rev Genet 5:169–178 [View Article][PubMed]
    [Google Scholar]
  33. 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 [View Article][PubMed]
    [Google Scholar]
  34. Morita T., Mochizuki Y., Aiba H. ( 2006). Translational repression is sufficient for gene silencing by bacterial small noncoding RNAs in the absence of mRNA destruction. Proc Natl Acad Sci U S A 103:4858–4863 [View Article][PubMed]
    [Google Scholar]
  35. Müller M., Weigand J. E., Weichenrieder O., Suess B. ( 2006). Thermodynamic characterization of an engineered tetracycline-binding riboswitch. Nucleic Acids Res 34:2607–2617 [View Article][PubMed]
    [Google Scholar]
  36. Ng-Ying-Kin N. M., Yaphe W. ( 1972). Properties of agar: parameters affecting gel-formation and the agarose–iodine reaction. Carbohydr Res 25:379–385 [View Article][PubMed]
    [Google Scholar]
  37. Pánek J., Bobek J., Mikulík K., Basler M., Vohradský J. ( 2008). Biocomputational prediction of small non-coding RNAs in Streptomyces . BMC Genomics 9:217 [View Article][PubMed]
    [Google Scholar]
  38. Parro V., Mellado R. P. ( 1993). Heterologous recognition in vivo of promoter sequences from the Streptomyces coelicolor dagA gene. FEMS Microbiol Lett 106:347–356 [View Article][PubMed]
    [Google Scholar]
  39. Parro V., Mellado R. P. ( 1994). Effect of glucose on agarase overproduction by Streptomyces . Gene 145:49–55 [View Article][PubMed]
    [Google Scholar]
  40. Pfeiffer V., Papenfort K., Lucchini S., Hinton J. C. D., Vogel J. ( 2009). Coding sequence targeting by MicC RNA reveals bacterial mRNA silencing downstream of translational initiation. Nat Struct Mol Biol 16:840–846 [View Article][PubMed]
    [Google Scholar]
  41. Reuther J., Wohlleben W. ( 2007). Nitrogen metabolism in Streptomyces coelicolor: transcriptional and post-translational regulation. J Mol Microbiol Biotechnol 12:139–146 [View Article][PubMed]
    [Google Scholar]
  42. Rodríguez-García A., Combes P., Pérez-Redondo R., Smith M. C. A., Smith M. C. M. ( 2005). Natural and synthetic tetracycline-inducible promoters for use in the antibiotic-producing bacteria Streptomyces . Nucleic Acids Res 33:e87 [View Article][PubMed]
    [Google Scholar]
  43. Servín-González L., Jensen M. R., White J., Bibb M. ( 1994). Transcriptional regulation of the four promoters of the agarase gene (dagA) of Streptomyces coelicolor A3(2). Microbiology 140:2555–2565 [View Article][PubMed]
    [Google Scholar]
  44. Sharma C. M., Vogel J. ( 2009). Experimental approaches for the discovery and characterization of regulatory small RNA. Curr Opin Microbiol 12:536–546 [View Article][PubMed]
    [Google Scholar]
  45. Sharma C. M., Darfeuille F., Plantinga T. H., Vogel J. ( 2007). A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes Dev 21:2804–2817 [View Article][PubMed]
    [Google Scholar]
  46. Sittka A., Lucchini S., Papenfort K., Sharma C. M., Rolle K., Binnewies T. T., Hinton J. C. D., Vogel J. ( 2008). Deep sequencing analysis of small noncoding RNA and mRNA targets of the global post-transcriptional regulator, Hfq. PLoS Genet 4:e1000163 [View Article][PubMed]
    [Google Scholar]
  47. Storz G., Altuvia S., Wassarman K. M. ( 2005). An abundance of RNA regulators. Annu Rev Biochem 74:199–217 [View Article][PubMed]
    [Google Scholar]
  48. Sun X., Zhulin I., Wartell R. M. ( 2002). Predicted structure and phyletic distribution of the RNA-binding protein Hfq. Nucleic Acids Res 30:3662–3671 [View Article][PubMed]
    [Google Scholar]
  49. Swiercz J. P., Hindra, Bobek J., Bobek J., Haiser H. J., Di Berardo C., Tjaden B., Elliot M. A. ( 2008). Small non-coding RNAs in Streptomyces coelicolor . Nucleic Acids Res 36:7240–7251 [View Article][PubMed]
    [Google Scholar]
  50. Tezuka T., Hara H., Ohnishi Y., Horinouchi S. ( 2009). Identification and gene disruption of small noncoding RNAs in Streptomyces griseus . J Bacteriol 191:4896–4904 [View Article][PubMed]
    [Google Scholar]
  51. Udekwu K. I., Darfeuille F., Vogel J., Reimegård J., Holmqvist E., Wagner E. G. H. ( 2005). Hfq-dependent regulation of OmpA synthesis is mediated by an antisense RNA. Genes Dev 19:2355–2366 [View Article][PubMed]
    [Google Scholar]
  52. Unoson C., Wagner E. G. H. ( 2008). A small SOS-induced toxin is targeted against the inner membrane in Escherichia coli . Mol Microbiol 70:258–270 [View Article][PubMed]
    [Google Scholar]
  53. Večerek 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 [View Article][PubMed]
    [Google Scholar]
  54. Vockenhuber M.-P., Sharma C. M., Statt M. G., Schmidt D., Xu Z., Dietrich S., Liesegang H., Mathews D. H., Suess B. ( 2011). Deep sequencing-based identification of small non-coding RNAs in Streptomyces coelicolor . RNA Biol 8:468–477 [View Article][PubMed]
    [Google Scholar]
  55. Vogel J. ( 2009). A rough guide to the non-coding RNA world of Salmonella . Mol Microbiol 71:1–11 [View Article][PubMed]
    [Google Scholar]
  56. Vogel J., Luisi B. F. ( 2011). Hfq and its constellation of RNA. Nat Rev Microbiol 9:578–589 [View Article][PubMed]
    [Google Scholar]
  57. Vogel J., Wagner E. G. H. ( 2007). Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol 10:262–270 [View Article][PubMed]
    [Google Scholar]
  58. Vogel J., Argaman L., Wagner E. G. H., Altuvia S. ( 2004). The small RNA IstR inhibits synthesis of an SOS-induced toxic peptide. Curr Biol 14:2271–2276 [View Article][PubMed]
    [Google Scholar]
  59. Walker S. C., Avis J. M., Conn G. L. ( 2003). General plasmids for producing RNA in vitro transcripts with homogeneous ends. Nucleic Acids Res 31:e82 [View Article][PubMed]
    [Google Scholar]
  60. Waters L. S., Storz G. ( 2009). Regulatory RNAs in bacteria. Cell 136:615–628 [View Article][PubMed]
    [Google Scholar]
  61. Watve M. G., Tickoo R., Jog M. M., Bhole B. D. ( 2001). How many antibiotics are produced by the genus Streptomyces?. Arch Microbiol 176:386–390 [View Article][PubMed]
    [Google Scholar]
  62. Wehmeier U. F. ( 1995). New multifunctional Escherichia coliStreptomyces shuttle vectors allowing blue-white screening on XGal plates. Gene 165:149–150 [View Article][PubMed]
    [Google Scholar]
  63. Widdick D. A., Eijlander R. T., van Dijl J. M., Kuipers O. P., Palmer T. ( 2008). A facile reporter system for the experimental identification of twin-arginine translocation (Tat) signal peptides from all kingdoms of life. J Mol Biol 375:595–603 [View Article][PubMed]
    [Google Scholar]
  64. Will S., Reiche K., Hofacker I. L., Stadler P. F., Backofen R. ( 2007). Inferring noncoding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput Biol 3:e65 [View Article][PubMed]
    [Google Scholar]
  65. Yamasaki M., Redenbach M., Kinashi H. ( 2001). Integrated structures of the linear plasmid SCP1 in two bidirectional donor strains of Streptomyces coelicolor A3(2). Mol Gen Genet 264:634–642 [View Article][PubMed]
    [Google Scholar]
  66. Zhang A., Wassarman K. M., Rosenow C., Tjaden B. C., Storz G., Gottesman S. ( 2003). Global analysis of small RNA and mRNA targets of Hfq. Mol Microbiol 50:1111–1124 [View Article][PubMed]
    [Google Scholar]
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