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J Bacteriol. 1997 Jun; 179(11): 3619–3624.
PMCID: PMC179156

Growth phase-dependent transcription of the Streptomyces ramocissimus tuf1 gene occurs from two promoters.


The str operon of Streptomyces ramocissimus contains the genes for ribosomal proteins S12 (rpsL) and S7 (rpsG) and for the polypeptide chain elongation factors G (EF-G) (fus) and Tu (EF-Tu) (tuf). This kirromycin producer contains three tuf or tuf-like genes; tuf1 encodes the regular EF-Tu and is located immediately downstream of fus. In vivo and in vitro transcription analysis revealed a transcription start site directly upstream of S. ramocissimus tuf1, in addition to the operon promoter rpsLp. Transcription from these promoters appeared to be growth phase dependent, diminishing drastically upon entry into stationary phase and at the onset of production of the EF-Tu-targeted antibiotic kirromycin. In surface-grown cultures, a second round of tuf1 transcription, coinciding with aerial mycelium formation and kirromycin production, was observed. The tuf1-specific promoter (tuf1p) was located in the intercistronic region between fus and tuf1 by high-resolution S1 mapping, in vitro transcription, and in vivo promoter probing. During logarithmic growth, the tuf1p and rpsLp transcripts are present at comparable levels. In contrast to Escherichia coli, which has two almost identical tuf genes, the gram-positive S. ramocissimus contains only tuf1 for its regular EF-Tu. High levels of EF-Tu may therefore be achieved by the compensatory activity of tuf1p.

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Selected References

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  • Alderson G, Ritchie DA, Cappellano C, Cool RH, Ivanova NM, Huddleston AS, Flaxman CS, Kristufek V, Lounes A. Physiology and genetics of antibiotic production and resistance. Res Microbiol. 1993 Oct;144(8):665–672. [PubMed]
  • An G, Friesen JD. The nucleotide sequence of tufB and four nearby tRNA structural genes of Escherichia coli. Gene. 1980 Dec;12(1-2):33–39. [PubMed]
  • An G, Lee JS, Friesen JD. Evidence for an internal promoter preceding tufA in the str operon of Escherichia coli. J Bacteriol. 1982 Feb;149(2):548–553. [PMC free article] [PubMed]
  • Bourn WR, Babb B. Computer assisted identification and classification of streptomycete promoters. Nucleic Acids Res. 1995 Sep 25;23(18):3696–3703. [PMC free article] [PubMed]
  • Brown KL, Wood S, Buttner MJ. Isolation and characterization of the major vegetative RNA polymerase of Streptomyces coelicolor A3(2); renaturation of a sigma subunit using GroEL. Mol Microbiol. 1992 May;6(9):1133–1139. [PubMed]
  • Buttner MJ. RNA polymerase heterogeneity in Streptomyces coelicolor A3(2). Mol Microbiol. 1989 Nov;3(11):1653–1659. [PubMed]
  • Chakraburtty R, White J, Takano E, Bibb M. Cloning, characterization and disruption of a (p)ppGpp synthetase gene (relA) of Streptomyces coelicolor A3(2). Mol Microbiol. 1996 Jan;19(2):357–368. [PubMed]
  • Clayton TM, Bibb MJ. Streptomyces promoter-probe plasmids that utilise the xylE gene of Pseudomonas putida. Nucleic Acids Res. 1990 Feb 25;18(4):1077–1077. [PMC free article] [PubMed]
  • Douglas SE. Unusual organization of a ribosomal protein operon in the plastid genome of Cryptomonas phi: evolutionary considerations. Curr Genet. 1991 Apr;19(4):289–294. [PubMed]
  • Feinberg AP, Vogelstein B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem. 1983 Jul 1;132(1):6–13. [PubMed]
  • Filer D, Furano AV. Duplication of the tuf gene, which encodes peptide chain elongation factor Tu, is widespread in Gram-negative bacteria. J Bacteriol. 1981 Dec;148(3):1006–1011. [PMC free article] [PubMed]
  • Gramajo HC, Takano E, Bibb MJ. Stationary-phase production of the antibiotic actinorhodin in Streptomyces coelicolor A3(2) is transcriptionally regulated. Mol Microbiol. 1993 Mar;7(6):837–845. [PubMed]
  • Granozzi C, Billetta R, Passantino R, Sollazzo M, Puglia AM. A breakdown in macromolecular synthesis preceding differentiation in Streptomyces coelicolor A3(2). J Gen Microbiol. 1990 Apr;136(4):713–716. [PubMed]
  • Hughes D. Both genes for EF-Tu in Salmonella typhimurium are individually dispensable for growth. J Mol Biol. 1990 Sep 5;215(1):41–51. [PubMed]
  • Jaskunas SR, Lindahl L, Nomura M. Identification of two copies of the gene for the elongation factor EF-Tu in E. coli. Nature. 1975 Oct 9;257(5526):458–462. [PubMed]
  • Lechner K, Heller G, Böck A. Organization and nucleotide sequence of a transcriptional unit of Methanococcus vannielii comprising genes for protein synthesis elongation factors and ribosomal proteins. J Mol Evol. 1989 Jul;29(1):20–27. [PubMed]
  • Lee JS, An G, Friesen JD, Fill NP. Location of the tufB promoter of E. coli: cotranscription of tufB with four transfer RNA genes. Cell. 1981 Jul;25(1):251–258. [PubMed]
  • Lonetto MA, Brown KL, Rudd KE, Buttner MJ. Analysis of the Streptomyces coelicolor sigE gene reveals the existence of a subfamily of eubacterial RNA polymerase sigma factors involved in the regulation of extracytoplasmic functions. Proc Natl Acad Sci U S A. 1994 Aug 2;91(16):7573–7577. [PMC free article] [PubMed]
  • MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH, MacNeil T. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene. 1992 Feb 1;111(1):61–68. [PubMed]
  • Mikulík K, Zhulanova E. Sequencing of the tuf1 gene and the phosphorylation pattern of EF-Tu1 during development and differentiation in Streptomyces collinus producing kirromycin. Biochem Biophys Res Commun. 1995 Aug 15;213(2):454–461. [PubMed]
  • Miller DL. A comparison of the activities of the products of the two genes for elongation factor Tu. Mol Gen Genet. 1978 Feb 7;159(1):57–62. [PubMed]
  • Murray MG. Use of sodium trichloroacetate and mung bean nuclease to increase sensitivity and precision during transcript mapping. Anal Biochem. 1986 Oct;158(1):165–170. [PubMed]
  • Post LE, Nomura M. DNA sequences from the str operon of Escherichia coli. J Biol Chem. 1980 May 25;255(10):4660–4666. [PubMed]
  • Sela S, Yogev D, Razin S, Bercovier H. Duplication of the tuf gene: a new insight into the phylogeny of eubacteria. J Bacteriol. 1989 Jan;171(1):581–584. [PMC free article] [PubMed]
  • Strauch E, Takano E, Baylis HA, Bibb MJ. The stringent response in Streptomyces coelicolor A3(2). Mol Microbiol. 1991 Feb;5(2):289–298. [PubMed]
  • Strohl WR. Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res. 1992 Mar 11;20(5):961–974. [PMC free article] [PubMed]
  • Summerton J, Atkins T, Bestwick R. A rapid method for preparation of bacterial plasmids. Anal Biochem. 1983 Aug;133(1):79–84. [PubMed]
  • Van Delft JH, Schmidt DS, Bosch L. The tRNA-tufB operon transcription termination and processing upstream from tufB. J Mol Biol. 1987 Oct 20;197(4):647–657. [PubMed]
  • van der Meide PH, Vijgenboom E, Talens A, Bosch L. The role of EF-Tu in the expression of tufA and tufB genes. Eur J Biochem. 1983 Feb 1;130(2):397–407. [PubMed]
  • van Wezel GP, Woudt LP, Vervenne R, Verdurmen ML, Vijgenboom E, Bosch L. Cloning and sequencing of the tuf genes of Streptomyces coelicolor A3(2). Biochim Biophys Acta. 1994 Oct 18;1219(2):543–547. [PubMed]
  • van Wezel GP, Krab IM, Douthwaite S, Bibb MJ, Vijgenboom E, Bosch L. Transcription analysis of the Streptomyces coelicolor A3(2) rrnA operon. Microbiology. 1994 Dec;140(Pt 12):3357–3365. [PubMed]
  • van Wezel GP, Takano E, Vijgenboom E, Bosch L, Bibb MJ. The tuf3 gene of Streptomyces coelicolor A3(2) encodes an inessential elongation factor Tu that is apparently subject to positive stringent control. Microbiology. 1995 Oct;141(Pt 10):2519–2528. [PubMed]
  • Vijgenboom E, Woudt LP, Heinstra PW, Rietveld K, van Haarlem J, van Wezel GP, Shochat S, Bosch L. Three tuf-like genes in the kirromycin producer Streptomyces ramocissimus. Microbiology. 1994 Apr;140(Pt 4):983–998. [PubMed]
  • Wright F, Bibb MJ. Codon usage in the G+C-rich Streptomyces genome. Gene. 1992 Apr 1;113(1):55–65. [PubMed]
  • Yanisch-Perron C, Vieira J, Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. [PubMed]
  • Yokota T, Sugisaki H, Takanami M, Kaziro Y. The nucleotide sequence of the cloned tufA gene of Escherichia coli. Gene. 1980 Dec;12(1-2):25–31. [PubMed]
  • Zengel JM, Lindahl L. A secondary promoter for elongation factor Tu synthesis in the str ribosomal protein operon of Escherichia coli. Mol Gen Genet. 1982;185(3):487–492. [PubMed]
  • Zengel JM, Archer RH, Lindahl L. The nucleotide sequence of the Escherichia coli fus gene, coding for elongation factor G. Nucleic Acids Res. 1984 Feb 24;12(4):2181–2192. [PMC free article] [PubMed]
  • Zengel JM, Lindahl L. Mapping of two promoters for elongation factor Tu within the structural gene for elongation factor G. Biochim Biophys Acta. 1990 Aug 27;1050(1-3):317–322. [PubMed]
  • Zukowski MM, Gaffney DF, Speck D, Kauffmann M, Findeli A, Wisecup A, Lecocq JP. Chromogenic identification of genetic regulatory signals in Bacillus subtilis based on expression of a cloned Pseudomonas gene. Proc Natl Acad Sci U S A. 1983 Feb;80(4):1101–1105. [PMC free article] [PubMed]

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