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PMID: 10322002 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phosphate control of oxytetracycline production by Streptomyces rimosus is at the level of transcription from promoters overlapped by tandem repeats similar to those of the DNA-binding sites of the OmpR family.

Journal of bacteriology ·Vol. 181 ·No. 10 ·1999-05-00 ·Pages 3025-32

McDowall KJ, Thamchaipenet A, Hunter IS

Abstract

Physiological studies have shown that Streptomyces rimosus produces the polyketide antibiotic oxytetracycline abundantly when its mycelial growth is limited by phosphate starvation. We show here that transcripts originating from the promoter for one of the biosynthetic genes, otcC (encoding anhydrotetracycline oxygenase), and from a promoter for the divergent otcX genes peak in abundance at the onset of antibiotic production induced by phosphate starvation, indicating that the synthesis of oxytetracycline is controlled, at least in part, at the level of transcription. Furthermore, analysis of the sequences of the promoters for otcC, otcX, and the polyketide synthase (otcY) genes revealed tandem repeats having significant similarity to the DNA-binding sites of ActII-Orf4 and DnrI, which are Streptomyces antibiotic regulatory proteins (SARPs) related to the OmpR family of transcription activators. Together, the above results suggest that oxytetracycline production by S. rimosus requires a SARP-like transcription factor that is either produced or activated or both under conditions of low phosphate concentrations. We also provide evidence consistent with the otrA resistance gene being cotranscribed with otcC as part of a polycistronic message, suggesting a simple mechanism of coordinate regulation which ensures that resistance to the antibiotic increases in proportion to production.

MeSH Terms
Bacterial Proteins Base Sequence Binding Sites DNA-Binding Proteins/metabolism Gene Expression Regulation, Bacterial Genes/genetics Genes, Bacterial/genetics Molecular Sequence Data Oxytetracycline/biosynthesis Phosphates/metabolism Promoter Regions, Genetic/genetics RNA, Bacterial/genetics RNA, Messenger/analysis,genetics,metabolism Response Elements/genetics Sequence Alignment Streptomyces/genetics,growth & development,metabolism Tandem Repeat Sequences/genetics Trans-Activators/genetics,metabolism Transcription, Genetic/genetics
Chemicals
Bacterial Proteins DNA-Binding Proteins Phosphates RNA, Bacterial RNA, Messenger Trans-Activators osmolarity response regulator proteins Oxytetracycline
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
McDowall K J
Faculty of Biological Sciences, University of Leeds, Leeds LS2 9JT, United Kingdom.
Thamchaipenet A
Hunter I S
References (35)
35 references, click to expand
  1. Compilation and analysis of DNA sequences associated with apparent streptomycete promoters.
    Nucleic Acids Res. 1992 Mar 11;20(5):961-74 PMID: 1549509
  2. Mapping of gene transcripts by nuclease protection assays and cDNA primer extension.
    Methods Enzymol. 1987;152:611-32 PMID: 2821358
  3. Structural relationships in the OmpR family of winged-helix transcription factors.
    J Mol Biol. 1997 Jun 13;269(3):301-12 PMID: 9199401
  4. Control of antibiotic biosynthesis.
    Microbiol Rev. 1980 Jun;44(2):230-51 PMID: 6991900
  5. Cloning and expression of a p-aminobenzoic acid synthetase gene of the candicidin-producing Streptomyces griseus.
    Gene. 1983 Nov;25(1):119-32 PMID: 6420235
  6. Regulation of glutamine synthetase in Streptomyces coelicolor.
    J Bacteriol. 1989 May;171(5):2378-83 PMID: 2468647
  7. Regulation of secondary metabolism in Streptomyces spp. and overproduction of daunorubicin in Streptomyces peucetius.
    J Bacteriol. 1992 Jan;174(1):144-54 PMID: 1729206
  8. Phosphate control of pabS gene transcription during candicidin biosynthesis.
    Gene. 1990 Sep 1;93(1):79-84 PMID: 1699847
  9. The act cluster contains regulatory and antibiotic export genes, direct targets for translational control by the bldA tRNA gene of Streptomyces.
    Cell. 1991 Aug 23;66(4):769-80 PMID: 1878971
  10. RNA polymerase heterogeneity in Streptomyces coelicolor.
    Nature. 1985 Jan 3-9;313(5997):22-7 PMID: 2578216
  11. Cloning and heterologous expression in Streptomyces lividans of Streptomyces rimosus genes involved in oxytetracycline biosynthesis.
    J Bacteriol. 1989 Feb;171(2):887-95 PMID: 2914874
  12. Characterization and regulation of p-aminobenzoic acid synthase from Streptomyces griseus.
    J Gen Microbiol. 1985 Jun;131(6):1279-87 PMID: 3930655
  13. Isolation of deoxyribonucleic acid and ribosomal ribonucleic acid from bacteria.
    Biochem J. 1967 Jul;104(1):258-62 PMID: 4962318
  14. Molecular cloning of resistance genes and architecture of a linked gene cluster involved in biosynthesis of oxytetracycline by Streptomyces rimosus.
    Mol Gen Genet. 1989 Jan;215(2):231-8 PMID: 2710100
  15. Nucleotide sequence of the phoB gene, the positive regulatory gene for the phosphate regulon of Escherichia coli K-12.
    J Mol Biol. 1986 Jul 5;190(1):37-44 PMID: 3537313
  16. Involvement of phosphotransacetylase, acetate kinase, and acetyl phosphate synthesis in control of the phosphate regulon in Escherichia coli.
    J Bacteriol. 1992 Apr;174(7):2124-30 PMID: 1551836
  17. DNA binding of PhoB and its interaction with RNA polymerase.
    J Mol Biol. 1996 May 31;259(1):15-26 PMID: 8648643
  18. Cloning and characterization of a phosphate-regulated promoter involved in phosphate control of candicidin biosynthesis.
    Gene. 1989 Jun 30;79(1):47-58 PMID: 2550329
  19. Nucleotide sequence, transcription and deduced function of a gene involved in polyketide antibiotic synthesis in Streptomyces coelicolor.
    Gene. 1988 Dec 30;74(2):305-20 PMID: 2469622
  20. A novel family of proteins that regulates antibiotic production in streptomycetes appears to contain an OmpR-like DNA-binding fold.
    Mol Microbiol. 1997 Sep;25(6):1181-4 PMID: 9350875
  21. Purification and characterization of the DNA-binding protein DnrI, a transcriptional factor of daunorubicin biosynthesis in Streptomyces peucetius.
    Mol Microbiol. 1996 Dec;22(5):801-13 PMID: 8971703
  22. Regulation of the phosphate regulon of Escherichia coli. Activation of pstS transcription by PhoB protein in vitro.
    J Mol Biol. 1988 Sep 5;203(1):85-95 PMID: 3054125
  23. Compilation and analysis of Escherichia coli promoter DNA sequences.
    Nucleic Acids Res. 1983 Apr 25;11(8):2237-55 PMID: 6344016
  24. Sequences of the oxytetracycline polyketide synthase-encoding otc genes from Streptomyces rimosus.
    Gene. 1994 Apr 8;141(1):141-2 PMID: 8163168
  25. Molecular cloning of tetracycline resistance genes from Streptomyces rimosus in Streptomyces griseus and characterization of the cloned genes.
    J Bacteriol. 1985 Mar;161(3):1010-6 PMID: 2982781
  26. Nutrient effects on anthracycline production by Streptomyces peucetius in a defined medium.
    Can J Microbiol. 1985 Mar;31(3):287-94 PMID: 3859358
  27. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors.
    Gene. 1985;33(1):103-19 PMID: 2985470
  28. Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated.
    Mol Microbiol. 1993 Mar;7(6):837-45 PMID: 7683365
  29. Protein phosphorylation and regulation of adaptive responses in bacteria.
    Microbiol Rev. 1989 Dec;53(4):450-90 PMID: 2556636
  30. Phosphate control sequences involved in transcriptional regulation of antibiotic biosynthesis.
    Trends Biotechnol. 1990 Jul;8(7):184-9 PMID: 1366623
  31. Regulation of ACV synthetase in penicillin- and cephalosporin-producing microorganisms.
    Biotechnol Adv. 1991;9(4):623-41 PMID: 14542052
  32. Control of bacterial alkaline phosphatase synthesis and variation in an Escherichia coli K-12 phoR mutant by adenyl cyclase, the cyclic AMP receptor protein, and the phoM operon.
    J Bacteriol. 1988 Mar;170(3):1092-102 PMID: 3277944
  33. At least three different RNA polymerase holoenzymes direct transcription of the agarase gene (dagA) of Streptomyces coelicolor A3(2).
    Cell. 1988 Feb 26;52(4):599-607 PMID: 3342448
  34. An integrated approach to studying regulation of production of the antibiotic methylenomycin by Streptomyces coelicolor A3(2).
    J Bacteriol. 1992 Mar;174(5):1487-94 PMID: 1537793
  35. Characterization of an oxytetracycline-resistance gene, otrA, of Streptomyces rimosus.
    Mol Microbiol. 1991 Dec;5(12):2923-33 PMID: 1809836
Article Info
Journal
Journal of bacteriology
Abbr.
J Bacteriol
ISSN
0021-9193
Published
1999-05-00
Pages
3025-32
Language
English
Region
United States
NLM ID
2985120R
PMCID
PMC93756
Subset
IM
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