1887

Abstract

The gene, encoding the enzyme polynucleotide phosphorylase (PNPase), was overexpressed in the actinomycin producer . Integration of pIJ8600, bearing the thiostrepton-inducible promoter, and its derivatives containing into the chromosome dramatically increased the growth rate of the resulting strains as compared with the parent strain. Thiostrepton induction of a strain containing pJSE340, bearing with a 5′-flanking region containing an endogenous promoter, led to a 2·5–3 fold increase in PNPase activity levels, compared with controls. Induction of a strain containing pJSE343, with only the ORF and some 3′-flanking sequence, led to lower levels of PNPase activity and a different pattern of expression compared with pJSE340. Induction of from pJSE340 resulted in a decrease in the chemical half-life of bulk mRNA and a decrease in poly(A) tail length as compared to RNAs from controls. Actinomycin production decreased in strains overexpressing as compared with controls but it was not possible to attribute this decrease specifically to the increase in PNPase levels. Overexpression of had no effect on ppGpp levels in the relevant strains. It was observed that the 3′-tails associated with RNAs from are heteropolymeric. The authors argue that those tails are synthesized by PNPase rather than by a poly(A) polymerase similar to that found in and that PNPase may be the sole RNA 3′-polynucleotide polymerase in streptomycetes.

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2003-08-01
2020-08-06
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References

  1. Adamis T., Champness W.. 1992; Genetic analysis of absB , a Streptomyces coelicolor locus involved in global antibiotic regulation. J Bacteriol174:4622–4628
    [Google Scholar]
  2. Bralley P., Jones G. H.. 2001; Poly(A) polymerase activity and RNA polyadenylation in Streptomyces coelicolor A3(2. Mol Microbiol40:1155–1164
    [Google Scholar]
  3. Bralley P., Jones G. H.. 2002; cDNA cloning confirms the polyadenylation of RNA decay intermediates in Streptomyces coelicolor . Microbiology148:1421–1425
    [Google Scholar]
  4. Cao G. J., Sarkar N.. 1992; Identification of the gene for an Escherichia coli poly(A) polymerase. Proc Natl Acad Sci U S A89:10380–10384
    [Google Scholar]
  5. Cashel M., Gentry D. R., Hernandez V. J., Vinella D.. others 1996; The stringent response. In Escherichia coli and Salmonella: Cellular and Molecular Biology pp1458–1496 Edited by Neidhardt F. C.. Washington, DC: American Society for Microbiology;
  6. Chakraburtty R., Bibb M. J.. 1997; The ppGpp synthetase gene ( relA ) of Streptomyces coelicolor A3(2) plays a conditional role in antibiotic production and morphological differentiation. J Bacteriol179:5854–5864
    [Google Scholar]
  7. Chakraburtty R., White J., Takano E., Bibb M. J.. 1996; Cloning and characterization and disruption of a (p)ppGpp synthetase gene ( relA ) of Streptomyces coelicolor A3(2). Mol Microbiol19:357–368
    [Google Scholar]
  8. Coburn G. A., Mackie G. A.. 1999; Degradation of mRNA in Escherichia coli : an old problem with some new twists. Prog Nucleic Acids Res Mol Biol62:55–105
    [Google Scholar]
  9. Combes P., Till R., Bee S., Smith M. C. M.. 2002; The Streptomyces genome contains multiple pseudo- attB sites for the ϕ C-31-encoded site-specific recombination system. J Bacteriol184:5746–5752
    [Google Scholar]
  10. Deutscher M., Reuven N. B.. 1991; Enzymatic basis for hydrolytic versus phosphorolytic mRNA degradation in Escherichia coli and Bacillus subtilis . Proc Natl Acad Sci U S A88:3277–3280
    [Google Scholar]
  11. Farr G. A., Oussenko I. A., Bechhofer D. H.. 1999; Protection against 3′-to-5′-RNA decay in Bacillus subtilis . J Bacteriol181:7323–7330
    [Google Scholar]
  12. Gallo M., Katz E.. 1972; Regulation of secondary metabolite biosynthesis: catabolite repression of phenoxazinone synthase and actinomycin production by glucose. J Bacteriol109:659–667
    [Google Scholar]
  13. Ghosh S., Deutscher M.. 1999; Oligoribonuclease is an essential component of the mRNA degradation pathway. Proc Natl Acad Sci U S A96:4372–4377
    [Google Scholar]
  14. Godefroy-Colburn T., Grunberg-Manago M.. 1972; Polynucleotide phosphorylase. In The Enzymes vol. 7 pp533–574 Edited by Boyer H. D.. New York: Academic Press;
  15. Grunberg-Manago M.. 1999; Messenger RNA stability and its role in control of gene expression in bacteria and phages. Annu Rev Genet33:193–227
    [Google Scholar]
  16. Grunberg-Manago M., Ochoa S.. 1955; Enzymatic synthesis and breakdown of polynucleotides: polynucleotide phosphorylase. J Am Chem Soc77:3165–3166
    [Google Scholar]
  17. Hagege J. M., Cohen S. N.. 1997; A developmentally regulated Streptomyces endoribonuclease resembles ribonuclease of Escherichia coli . Mol Microbiol25:1077–1090
    [Google Scholar]
  18. Herskovitz M. A., Bechhofer D. H.. 2000; Endoribonuclease RNase III is essential in Bacillus subtilis . Mol Microbiol38:1027–1033
    [Google Scholar]
  19. Hesketh A., Sun J., Bibb M. J.. 2001; Induction of ppGpp synthesis in Streptomyces coelicolor A3(2) grown under conditions of nutritional sufficiency elicits actII-orf4 transcription and actinorhodin biosynthesis. Mol Microbiol39:136–141
    [Google Scholar]
  20. Holmes D. J., Caso J., Thompson C.. 1993; Autogenous transcriptional activation of a thiostrepton-induced gene in Streptomyces lividans . EMBO J12:3183–3191
    [Google Scholar]
  21. Hoyt S., Jones G. H.. 1999; relA is required for actinomycin production in Streptomyces antibioticus . J Bacteriol181:3824–3829
    [Google Scholar]
  22. Hsieh C.-J., Jones G. H.. 1995; Nucleotide sequence, transcriptional analysis and glucose regulation of the phenoxazinone synthase gene from Streptomyces antibioticus . J Bacteriol177:5740–5747
    [Google Scholar]
  23. Huang J., Lih C.-J., Pan K.-H., 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 Dev15:3183–3192
    [Google Scholar]
  24. Jarrige A.-C., Mathy N., Portier C.. 2001; PNPase autocontrols its expression by degrading a double-stranded structure in the pnp mRNA leader. EMBO J20:6845–6855
    [Google Scholar]
  25. Jarrige A.-C., Bréchemier-Baey D., Mathy N., Duché O., Portier C.. 2002; Mutational analysis of polynucleotide phosphorylase from Escherichia coli . J Mol Biol312:397–409
    [Google Scholar]
  26. Jones G. H.. 1994a; Purification and properties of ATP: GTP 3′-pyrophosphotransferase (guanosine pentaphosphate synthetase) from Streptomyces antibioticus . J Bacteriol176:1475–1481
    [Google Scholar]
  27. Jones G. H.. 1994b; Activation of ATP-GTP 3′-pyrophosphotransferase (guanosine pentaphosphate synthetase) in Streptomyces antibioticus . J Bacteriol176:1482–1487
    [Google Scholar]
  28. Jones G. H.. 2000; Actinomycin synthesis persists in a strain of Streptomyces antibioticus lacking phenoxazinone synthase. Antimicrob Agents Chemother44:1322–1327
    [Google Scholar]
  29. Jones G. H., Bibb M. J.. 1996; Guanosine pentaphosphate synthetase from Streptomyces antibioticus is also a polynucleotide phosphorylase. J Bacteriol178:4281–4288
    [Google Scholar]
  30. Jones G. H., Paget M. S. B., Chamberlin L., Buttner M. J.. 1997; Sigma-E is required for the production of the antibiotic actinomycin in Streptomyces antibioticus . Mol Microbiol23:169–178
    [Google Scholar]
  31. Kieser Y., Bibb M. J., Buttner M. J., Chater K. F., Hopwood D. A.. 2000; Practical Streptomyces Genetics Norwich, UK: John Innes Foundation;
  32. Lisitsky I., Klaff P., Schuster G.. 1996; Addition of destabilizing poly(A) rich sequences to endonuclease cleavage sites during the degradation of chloroplast RNA. Proc Natl Acad Sci U S A93:13398–13403
    [Google Scholar]
  33. Littauer U. Z., Soreq H.. 1982; Polynucleotide phosphorylase. In The Enzymes vol. 15 pp517–553 Edited by Boyer H. D. New York: Academic Press;
  34. Luttinger A., Hahn J., Dubnau D.. 1996; Polynucleotide phosphorylase is necessary for competence development in Bacillus subtilis . Mol Microbiol19:343–356
    [Google Scholar]
  35. Mohanty B. K., Kushner S. R.. 2000a; Polynucleotide phosphorylase, RNase II and RNase E play different roles in the in vivo modulation of polyadenylation in Escherichia coli . Mol Microbiol36:982–994
    [Google Scholar]
  36. Mohanty B. K., Kushner S. R.. 2000b; Polynucleotide phosphorylase functions both as a 3′-5′ exonuclease and a poly(A) polymerase in Escherichia coli . Proc Natl Acad Sci U S A97:11966–11971
    [Google Scholar]
  37. Ohnishi Y., Nishiyama Y., Sato R., Kameyama S., Horinouchi S.. 2000; An oligoribonuclease gene in Streptomyces griseus . J Bacteriol182:4647–4653
    [Google Scholar]
  38. Price B., Adamis T., Champness W.. 1999; A Streptomyces coelicolor antibiotic regulatory gene, absB , encodes an RNase III homolog. J Bacteriol181:6142–6151
    [Google Scholar]
  39. Rauhut R., Klug G.. 1999; mRNA degradation in bacteria. FEMS Microbiol Rev23:353–370
    [Google Scholar]
  40. Regnier P., Arraiano C. M.. 2000; Degradation of mRNA in bacteria: emergence of ubiquitous features. Bioessays22:235–244
    [Google Scholar]
  41. Rott R., Zipor G., Portnoy V., Liveanu V., Schuster G.. 2003; RNA polyadenylation and degradation in cyanobacteria are similar to the chloroplast but different from E. coli . J Biol Chem278:15771–15777
    [Google Scholar]
  42. Sun J., Kelemen G. H., Fernandez-Abalos J. M., Bibb M. J.. 1999; Green fluorescent protein as a reporter for spatial and temporal gene expression in Streptomyces coelicolor A3(2. Microbiology145:2221–2227
    [Google Scholar]
  43. Symmons M., Jones G. H., Luisi B.. 2000; A duplicated fold is the structural basis for polynucleotide phosphorylase catalytic activity, processivity and regulation. Structure8:1215–1226
    [Google Scholar]
  44. Takano E., Gramajo H. C., Strauch E., Andres N., White J., Bibb M. J.. 1992; Transcriptional regulation of the redD transcriptional activator gene accounts for growth-phase dependent production of the antibiotic undecylprodigiosin in Streptomyces coelicolor A3(2. Mol Microbiol6:2797–2804
    [Google Scholar]
  45. Vohradsky J., Li X. M., Dale G., Folcher M., Nguyen L., Viollier P. H., Thompson C. J.. 2000; Developmental control of stress stimulons in Streptomyces coelicolor revealed by statistical analysis of global gene expression patterns. J Bacteriol182:4979–4986
    [Google Scholar]
  46. Yehudai-Resheff S., Hirsh M., Schuster G.. 2001; Polynucleotide phosphorylase functions as both an exonuclease and a poly(A) polymerase in spinach chloroplasts. Mol Cell Biol21:5408–5416
    [Google Scholar]
  47. Zuo Y., Deutscher M.. 2001; Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res29:1017–1026
    [Google Scholar]
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