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Activity of translation system and abundance of tmRNA during development ofStreptomyces aureofaciens producing tetracycline

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Abstract

Transition from exponential phase of growth to stationary phase inStreptomyces aureofaciens is characterized by a decrease in the rate of translation and induction of tetracycline (Ttc) biosynthesis. In exponential phase, no significant changes were found in the activity of ribosomes at binding of ternary complex Phe-tRNA.EF-Tu.GTP to the A-site on ribosomes. Overexpression of Ttc in stationary phase is accompanied by a decrease in the binding of the ternary complex Phe-tRNA.EF-Tu.GTP to the A-site of ribosome and a formation of an aggregate with Ttc by part of the ribosomes. Antibiotics that cause ribosome to stall or pause could increase the requirement for tmRNA in the process calledtrans-translation. We found differences in the level of tmRNA during the development ofS. aureofaciens. Subinhibitory concentrations of Ttc, streptomycin and chloramphenicol induced an increase in the tmRNA level in cells from the exponential phase of growth.In vitro trans-translation system ofS. aureofaciens was sensitive to Ttc at a concentration of >15 µmol/L; thetrans-translation system can thus be considered to contribute to resistance against Ttc produced only at sublethal concentrations. These experiments suggest that the main role of the rising tmRNA level at the beginning of the Ttc production is connected with ribosome rescue.

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Abbreviations

Clm:

chloramphenicol

Kir:

kirromycin

Stm:

streptomycin

Ttc:

tetracycline

DTT:

1,4-dithiothreitol

tmRNA:

transfer-messenger RNA

References

  • Abo T., Ueda K., Sunohara T., Ogawa K., Aiba H.: SsrA-mediated protein tagging in the presence of miscoding drugs and its physiological role inEscherichia coli.Genes Cells 7, 629–638 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Asano K., Kurita D., Takada K., Konno T., Muto A., Himeno H.: Competition betweentrans-translation and termination or elongation of translation.Nucl.Acids Res. 33, 5544–5552 (2005).

    Article  CAS  PubMed  Google Scholar 

  • van Bogelen R.A., Neidhardt F.C.: Ribosomes as sensors of heat and cold shock inEscherichia coli.Proc.Nat.Acad.Sci.USA 87, 5589–5593 (1999).

    Article  Google Scholar 

  • Bralley P., Jones H.G.: Organization and expression of polynucleotide phosphorylase gene (pnp) ofStreptomyces: processing ofpnp transcripts inStreptomyces antibioticus.J.Bacteriol. 186, 3160–3172 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Braud S., Lavire C., Bellier A., Mazodier P.: Effect of SsrA (tmRNA) tagging system on translational regulation inStreptomyces.Arch.Microbiol. 184, 343–352 (2005).

    Article  PubMed  Google Scholar 

  • Brodersen D.E., Clemons W.M., Carter A.P., Morgan-Warren R.J., Wimberly B.T., Ramakrishnan V.R.: The structural basis for the action of antibiotics tetracycline, pactamycin and hygromycin B on the 30S ribosomal subunit.Cell 103, 1143–1154 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Collier J., Binet E., Bouloc P.: Competition between SsrA tagging and translational termination at weak stop codons inEscherichia coli.Mol.Microbiol. 45, 745–754 (2002).

    Article  CAS  PubMed  Google Scholar 

  • De la Cruz J., Vioque A.: Increased sensitivity to protein synthesis inhibitors in cells lacking tmRNA.RNA 7, 1708–1716 (2001).

    PubMed  Google Scholar 

  • Dantley K.A., Dannelly H.K., Burdett V.: Binding interaction between Tet(M) and the ribosome: requirements for binding.J.Bacteriol. 180, 4089–4092 (1998).

    CAS  PubMed  Google Scholar 

  • Hayes C.S., Bose B., Sauer R.T.: Stop codons preceded by rare arginine codons are efficient determinants of SsrA tagging inEscherichia coli.Proc.Nat.Acad.Sci.USA 99, 3440–3445 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Hayes C.S., Sauer R.T.: Cleavage of the A-site mRNA codon during ribosome pausing provides a mechanism for translation quality control.Mol.Cell. 12, 903–911 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Herman C., Thevenet D., Bouloc P., Walker G.C., D’Ari R.: Degradation of carboxy-terminal-tagged cytoplasmic proteins by theEscherichia coli proteinase HflB (FisH).Genes Dev. 12, 1348–1355 (1998).

    Article  CAS  PubMed  Google Scholar 

  • Himeno H., Sato M., Tadaki T., Fukushima M., Ushida C., Muto A.:In vitro trans-translation mediated by alanine-charged 10Sa RNA.J.Mol.Biol. 268, 803–808 (1997).

    Article  CAS  PubMed  Google Scholar 

  • Hong S.-J., Tran Q.-A., Keiler K.C.: Cell cycle regulated degradation of tmRNA is controlled by RnaseR and SmpB.Mol.Microbiol. 57, 565–575 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Huang C., Wolfgang M.C., Withey J., Koomey M., Friedman D.I.: Charged tmRNA but not tmRNA-mediated proteolysis is essential forNeisseria gonorrhoeae viability.EMBO J. 19, 1098–1107 (2002).

    Article  Google Scholar 

  • Hutchison C.A., Peterson S.N., Gill S.R., Cline R.T., White O., Fraser C.M., Smith H.O., Venter J.C.: Global transposon mutagenesis and a minimalMycoplasma genome.Science 286, 2165–2169 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Julio S.M., Heithof D.N., Mahan M.J.:ssrA (tmRNA) plays a role inSalmonella enterica serovar Typhimurium pathogenesis.J.Bacteriol. 182, 1558–1563 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Karzai A.W., Susskind M.M., Sauer R.T.: SmpB, a unique RNA-binding protein essential for the peptide-tagging activity of SsrA (tmRNA).EMBO J. 18, 3793–3799 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Karzai A.W., Sauer R.T.: Protein factors associated with the SsrA SmpB tagging and ribosome rescue complex.Proc.Nat.Acad.Sci.USA 98, 3040–3044 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Keiler K.C., Waller P.R., Sauer R.T.: Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA.Science 271, 990–993 (2000).

    Article  Google Scholar 

  • Keiler K.C., Shapiro L.: tmRNA is required for correct timing of DNA replication inCaulobacter crescentus.J.Bacteriol. 185, 573–580 (2003).

    Article  CAS  PubMed  Google Scholar 

  • Kieser T., Bibb M.J., Buttner M.J., Chater K.F., Hopwood D.A.:Practical Streptomycetes Genetics, pp. 54–55. John Innes Foundation, Norwich (UK) 2000.

    Google Scholar 

  • Konno T., Takahashi T., Kurita D., Muto A., Himeno H.: A minimum structure of aminoglycosides that causes an initiation shift oftrans-translation.Nucl.Acids Res. 32, 4119–4126 (2004).

    Article  CAS  PubMed  Google Scholar 

  • Li X., Hirano R., Tagami H., Aiba H.: Protein tagging at rare codons is caused by tmRNA action at 3′ end of nonstop mRNA generated in response to ribosome stalling.RNA 12, 248–255 (2005).

    Article  PubMed  Google Scholar 

  • Mikulík K., Jiraňová A., Weiser J., Janda I., Šťastná J., Quyen N.: Transalation of poly(U) on ribosomes fromStreptomyces aureofaciens.Biochim.Biophys.Acta. 740, 99–107 (1983).

    Google Scholar 

  • Munavar H., Zhou Y., Gottesman S.: Analysis of theEscherichia coli Alp phenotype heat shock induction inssrA mutants.J.Bacteriol. 187, 4739–4751 (2005).

    Article  CAS  PubMed  Google Scholar 

  • Murray V.: Improved double-stranded DNA sequencing using linear polymerase chain reaction.Nucl.Acids Res. 17, 8889 (1989).

    Article  CAS  PubMed  Google Scholar 

  • Muto A., Fujihara A., Ito K.I., Matsuno J., Ushida C., Himeno H.: Requirement of transfer-messenger RNA for growth ofBacillus subtilis under stresses.Genes Cells 5, 627–635 (2000).

    Article  CAS  PubMed  Google Scholar 

  • Palečková P., Felsberg J., Halada P., Bobek J., Mikulik K.: Structure of tmRNA ofStreptomycetes and association of proteins with tmRNA, p. 98 inAbstr. Book, 10th Internat. Symp. Genetics of Industrial Microorganisms. Inst. Microbiol. Acad. Sci. Czech Rep., Prague 2006.

    Google Scholar 

  • Pioletti M., Schlunzen F., Harms J., Zarivach R., Gluhmann M., Avila H., Bashan A., Bertels H., Auerbach T., Jacoby C., Hartsch T., Yonath A., Franceschi F.: Crystal structures of complexes of the small ribosomal subunit with tetracycline, edeine and IF3.EMBO J. 20, 1829–1839 (2001).

    Article  CAS  PubMed  Google Scholar 

  • Roberts M.C.: Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility and distribution.FEMS Microbiol.Rev. 19, 1–24 (1996).

    Article  CAS  PubMed  Google Scholar 

  • Roche E.D., Sauer R.T.: SsrA-mediated peptide tagging caused by rare codons and tRNA scarcity.EMBO J. 18, 4579–4589 (1999).

    Article  CAS  PubMed  Google Scholar 

  • Ross J.I., Eady E.A., Cove J.H., Cundliffe W.J.: 16S rRNA mutation associated with tetracycline resistance in a Gram-positive bacterium.Antimicrob.Agents Chemother. 42, 1702–1705 (1998).

    CAS  PubMed  Google Scholar 

  • Sanger F., Nickeln S., Coulson A.R.: DNA sequencing with chain-terminator inhibitors.Proc.Nat.Acad.Sci.USA 74, 5463–5467 (1977).

    Article  CAS  PubMed  Google Scholar 

  • Slavcev R.A., Hayes S.: Blocking the T4 lysis inhibition phenotype.Gene 321, 163–171 (2004).

    Article  Google Scholar 

  • Suarez G., Nathans D.: Inhibition of aminoacyl-sRNA binding to ribosomes by tetracycline.Biochem.Biophys.Res.Commun. 18, 743–750 (1965).

    Article  CAS  Google Scholar 

  • Ueda K., Yamamoto Y., Ogawa K., Abo T., Inokuchi H., Aiba H.: Bacterial SsrA system plays a role in coping with unwanted translational read through caused by suppressor tRNAs.Genes Cells 7, 509–519 (2002).

    Article  CAS  PubMed  Google Scholar 

  • Vioque A., de la Cruz J.:Trans-translation and protein synthesis inhibitors.FEMS Microbiol.Lett. 218, 9–14 (2003).

    Article  CAS  PubMed  Google Scholar 

Download references

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Authors and Affiliations

  1. Institute of Microbiology, Academy of Sciences of the Czech Republic, 142 20, Prague, Czechia

    P. Palečková, J. Bobek, J. Felsberg & K. Mikulík

Authors
  1. P. Palečková
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  2. J. Bobek
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  3. J. Felsberg
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  4. K. Mikulík
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Correspondence to K. Mikulík.

Additional information

This work was supported by grant of theGrant Agency of the Czech Republic no. 203/05/0106 to the corresponding author.

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Palečková, P., Bobek, J., Felsberg, J. et al. Activity of translation system and abundance of tmRNA during development ofStreptomyces aureofaciens producing tetracycline. Folia Microbiol 51, 517–524 (2006). https://doi.org/10.1007/BF02931615

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  • DOI: https://doi.org/10.1007/BF02931615

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