Skip to main content
Log in

RraAS1 inhibits the ribonucleolytic activity of RNase ES by interacting with its catalytic domain in Streptomyces coelicolor

  • Microbial Genetics, Genomics and Molecular Biology
  • Published:
Journal of Microbiology Aims and scope Submit manuscript

Abstract

RraA is a protein inhibitor of RNase E, which degrades and processes numerous RNAs in Escherichia coli. Streptomyces coelicolor also contains homologs of RNase E and RraA, RNase ES and RraAS1/RraAS2, respectively. Here, we report that, unlike other RraA homologs, RraAS1 directly interacts with the catalytic domain of RNase ES to exert its inhibitory effect. We further show that rraAS1 gene deletion in S. coelicolor results in a higher growth rate and increased production of actinorhodin and undecylprodigiosin, compared with the wild-type strain, suggesting that RraAS1-mediated regulation of RNase ES activity contributes to modulating the cellular physiology of S. coelicolor.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ahn, S., Shin, E., Yeom, J.H., and Lee, K. 2008. Modulation of Escherichia coli RNase E action by RraAS2, a Streptomyces coelicolor ortholog of RraA. Korean J. Microbiol. 44, 93–97.

    Google Scholar 

  • Callaghan, A.J., Aurikko, J.P., Ilag, L.L., Günter Grossmann, J., Chandran, V., Kühnel, K., Poljak, L., Carpousis, A.J., Robinson, C.V., Symmons, M.F., et al. 2004. Studies of the RNA degradosome- organizing domain of the Escherichia coli ribonuclease RNase E. J. Mol. Biol. 340, 965–979.

    Article  CAS  PubMed  Google Scholar 

  • Celesnik, H., Deana, A., and Belasco, J.G. 2007. Initiation of RNA decay in Escherichia coli by 5’pyrophosphate removal. Mol. Cell 27, 79–90.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, J., Lee, K., Zhao, M., Qiu, J., Zhan, X., Saxena, A., Moore, C.J., Cohen, S.N., and Georgiou, G. 2006. Differential modulation of E. coli mRNA abundance by inhibitory proteins that alter the composition of the degradosome. Mol. Microbiol. 61, 394–406.

    Article  CAS  PubMed  Google Scholar 

  • Ghora, B.K. and Apirion, D. 1978. Structural analysis and in vitro processing to p5 rRNA of a 9S RNA molecule isolated from an rne mutant of E. coli. Cell 15, 1055–1066.

    Article  CAS  PubMed  Google Scholar 

  • Górna, M.W., Pietras, Z., Tsai, Y.C., Callaghan, A.J., Hernandez, H., Robinson, C.V., and Luisi, B.F. 2010. The regulatory protein RraA modulates RNA-binding and helicase activities of the E. coli RNA degradosome. RNA 16, 553–562.

    Article  PubMed  PubMed Central  Google Scholar 

  • Gust, B., Kieser, T., and Chater, K. 2002. PCR targeting system in Streptomyces coelicolor A3(2). In Gust, B., Kieser, T., and Chater, K. (eds.), pp. 1–39. The John Innes Foundation, Norwich, UK.

    Google Scholar 

  • Hagege, J.M. and Cohen, S.N. 1997. A developmentally regulated Streptomyces endoribonuclease resembles ribonuclease E of Escherichia coli. Mol. Microbiol. 25, 1077–1090.

    Article  CAS  PubMed  Google Scholar 

  • Heo, J., Kim, D., Joo, M., Lee, B., Seo, S., Lee, J., Song, S., Yeom, J.H., Ha, N.C., and Lee, K. 2016a. RraAS2 requires both scaffold domains of RNase ES for high-affinity binding and inhibitory action on the ribonucleolytic activity. J. Microbiol. 54, 660–666.

    Article  CAS  PubMed  Google Scholar 

  • Heo, J., Seo, S., Lee, B., Yeom, J.H., and Lee, K. 2016b. Implications of Streptomyces coelicolor RraAS1 as an activator of ribonuclease activity of Escherichia coli RNase E. Korean J. Microbiol. 52, 243–248.

    Article  Google Scholar 

  • Huang, J., Lih, C.J., Pan, K.H., and Cohen, S.N. 2001. Global analysis of growth phase responsive gene expression and regulation of antibiotic biosynthetic pathways in Streptomyces coelicolor using DNA microarrays. Genes Dev. 15, 3183–3192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jain, C. and Belasco, J.G. 1995. RNase E autoregulates its synthesis by controlling the degradation rate of its own mRNA in Escherichia coli: unusual sensitivity of the rne transcript to RNase E activity. Genes Dev. 9, 84–96.

    Article  CAS  PubMed  Google Scholar 

  • Jeong, Y., Kim, J.N., Kim, M., Bucca, G., Cho, S., Yoon, Y., Kim, B.G., Roe, J.H., Kim, S., Smith, C.P., et al. The dynamic transcriptional and translational landscape of the model antibiotic producer Streptomyces coelicolor A3(2). Nat. Commun. 7, 11605.

  • Jiang, X. and Belasco, J.G. 2004. Catalytic activation of multimeric RNase E and RNase G by 5’-monophosphorylated RNA. Proc. Natl. Acad. Sci. USA 101, 9211–9216.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kido, M., Yamanaka, K., Mitani, T., Niki, H., Ogura, T., and Hiraga, S. 1996. RNase E polypeptides lacking a carboxyl-terminal half suppress a mukB mutation in Escherichia coli. J. Bacteriol. 178, 3917–3925.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. 2000. Practical Streptomyces genetics. In Kieser, T., Bibb, M.J., Buttner, M.J., Chater, K.F., and Hopwood, D.A. (eds.). The John Innes Foundation, Norwich, UK.

    Google Scholar 

  • Kim, D., Kim, Y.H., Jang, J., Yeom, J.H., Jun, J.W., Hyun, S., and Lee, K. 2016. Functional analysis of Vibrio vulnificus orthologs of Escherichia coli RraA and RNase E. Curr. Microbiol. 72, 716–722.

    Article  CAS  PubMed  Google Scholar 

  • Kim, J.M., Song, W.S., Kim, H.L., Go, H., and Lee, K. 2007. Identification and functional analysis of proteins interacting with Streptomyces coelicolor RNase ES. Korean J. Microbiol. 43, 72–75.

    Google Scholar 

  • Kime, L., Jourdan, S.S., Stead, J.A., Hidalgo-Sastre, A., and McDowall, K.J. 2010. Rapid cleavage of RNA by RNase E in the absence of 5????monophosphate stimulation. Mol. Microbiol. 76, 590–604.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K., Bernstein, J.A., and Cohen, S.N. 2002. RNase G complementation of rne null mutation identifies functional interrelationships with RNase E in Escherichia coli. Mol. Microbiol. 43, 1445–1456.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K. and Cohen, S.N. 2003. RNase E shows shuffling of catalytic and PNPase-binding domains. Mol. Microbiol. 48, 349–360.

    Article  CAS  PubMed  Google Scholar 

  • Lee, M., Yeom, J.H., Sim, S.H., Ahn, S., and Lee, K. 2009. RNase E in vivo. Curr. Microbiol. 58, 349–353.

    Article  CAS  PubMed  Google Scholar 

  • Lee, K., Zhan, X., Gao, J., Qiu, J., Feng, Y., Meganathan, R., Cohen, S.N., and Georgiou, G. 2003. RraA. a protein inhibitor of RNase E activity that globally modulates RNA abundance in E. coli. Cell 114, 623–634.

    Article  CAS  PubMed  Google Scholar 

  • Li, Z. and Deutscher, M.P. 2002. RNase E plays an essential role in the maturation of Escherichia coli tRNA precursors. RNA 8, 97–109.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mackie, G.A. 1998. Ribonuclease E is a 5’-end-dependent endonuclease. Nature 395, 720–723.

    Article  CAS  PubMed  Google Scholar 

  • McDowall, K.J. and Cohen, S.N. 1996. The N-terminal domain of the rne gene product has RNase E activity and is non-overlapping with the arginine-rich RNA-binding site. J. Mol. Biol. 255, 349–355.

    Article  CAS  PubMed  Google Scholar 

  • Mudd, E.A. and Higgins, C.F. 1993. Escherichia coli endoribonuclease RNase E: autoregulation of expression and site-specific cleavage of mRNA. Mol. Microbiol. 9, 557–568.

    Article  CAS  PubMed  Google Scholar 

  • Ow, M.C., Liu, Q., and Kushner, S.R. 2000. Analysis of mRNA decay and rRNA processing in Escherichia coli in the absence of RNase E-based degradosome assembly. Mol. Microbiol. 38, 854–866.

    Article  CAS  PubMed  Google Scholar 

  • Pietras, Z., Hardwick, S.W., Swiezewski, S., and Luisi, B.F. 2013. Potential regulatory interactions of Escherichia coli RraA protein with DEAD-box helicases. J. Biol. Chem. 288, 31919–31929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh, D., Chang, S.J., Lin, P.H., Averina, O.V., Kaberdin, V.R., and Lin-Chao, S. 2009. Regulation of ribonuclease E activity by the L4 ribosomal protein of Escherichia coli. Proc. Natl. Acad. Sci. USA 106, 864–869.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sousa, S., Marchand, I., and Dreyfus, M. 2001. Autoregulation allows Escherichia coli RNase E to adjust continuously its synthesis to that of its substrates. Mol. Microbiol. 42, 867–878.

    Article  CAS  PubMed  Google Scholar 

  • Vanzo, N.F., Li, Y.S., Py, B., Blum, E., Higgins, C.F., Raynal, L.C., Krisch, H.M., and Carpousis, A.J. 1998. Ribonuclease E organizes the protein interactions in the Escherichia coli RNA degradosome. Genes Dev. 12, 2770–2781.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yeom, J.H., Go, H., Shin, E., Kim, H.L., Han, S.H., Moore, C.J., Bae, J., and Lee, K. 2008a. Inhibitory effects of RraA and RraB on RNAse E-related enzymes imply conserved functions in the regulated enzymatic cleavage of RNA. FEMS Microbiol. Lett. 285, 10–15.

    Article  CAS  PubMed  Google Scholar 

  • Yeom, J.H. and Lee, K. 2006. RraA rescues Escherichia coli cells over-producing RNase E from growth arrest by modulating the ribonucleolytic activity. Biochem. Biophys. Res. Commun. 345, 1372–1376.

    Article  CAS  PubMed  Google Scholar 

  • Yeom, J.H., Shin, E., Go, H., Sim, S.H., Seong, M.J., and Lee, K. 2008b. Functional implications of the conserved action of regulators of ribonuclease activity. J. Microbiol. Biotechnol. 18, 1353–1356.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Ji-Hyun Yeom or Kangseok Lee.

Additional information

These authors contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Seo, S., Kim, D., Song, W. et al. RraAS1 inhibits the ribonucleolytic activity of RNase ES by interacting with its catalytic domain in Streptomyces coelicolor . J Microbiol. 55, 37–43 (2017). https://doi.org/10.1007/s12275-017-6518-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12275-017-6518-0

Keywords

Navigation