Abstract
Factor C is an extracellular signal protein involved in cellular differentiation in Streptomyces griseus. Nuclease S1 mapping experiments revealed that transcription of the gene takes place from a single promoter in a developmental-stage specific manner. The latter was also confirmed by in vivo promoter probing. The sequence of its promoter suggests that the gene is not transcribed by the major sigma factor. The cloned gene expressed from its own promoter in low- and high-copy-number vectors restored normal sporulation to a bald mutant of Streptomyces griseus. Computer analysis of the amino acid sequence revealed the presence of a transmembrane localization segment with the N-terminus positioned inside the cell. These data fit well into our working model that points at an important role for factor C in the morphogenesis of Streptomyces griseus.
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References
Babcock MJ & Kendrick KE (1988) Cloning of DNA involved in sporulation of Streptomyces griseus. J. Bacteriol. 170: 2802–2808
Birkó Zs, Sümegi A, Vinnai A, van Wezel GP, Szeszák F, Vitális S, Szabó P, Kele Z, Janáky T & Biró S (1999) Characterization of the gene for factor C, an extracellular signal protein involved in morphological differentiation of Streptomyces griseus. Microbiol. 145: 2245–2253
Biró S, Békési I, Vitális S & Szabó G (1980) A substance effecting differentiation in Streptomyces griseus. Eur. J. Biochem. 103: 359–363
Brown KL, Wood S & Buttner MJ (1992) Isolation and characterization of the major vegetative RNA polymerase of Streptomyces coelicolor A3(2); renaturation of a sigma subunit using GroEL. Mol. Microbiol. 6: 1133–1139
Chater KF (1989) Multilevel regulation of Streptomyces differentiation. Trends in Genetics 5: 372–377
Chater KF (1998) Taking a genetic scalpel to the Streptomyces colony. Microbiol. 144: 1465–1478
Cserzo M, Wallin E, Simon I, Von Heijne G & Elofsson A (1997) Prediction of transmembrane alpha helices in prokaryotic membrane proteins: the Dense Alignment Surface method. Prot. Eng. 10(6): 673–676
Floriano B & Bibb MJ (1996) afsR is a pleiotropic but conditionally required regulatory gene for antibiotic production in Streptomyces coelicolor A3(2). Mol. Microbiol. 21: 385–396
Hawley DK & McClure WR (1983) Compilation and analysis of Escherichia coli promoter DNA sequences. Nucleic Acids Res. 11: 2237–2255
Hofmann K & Stoffel W(1993) Tmbase-A database of membrane spanning proteins segments. Biol. Chem. Hoppe-Seyler 347: 166
Hopwood DA (1999) Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico. Microbiol. 145: 2183–2202
Hopwood DA, Bibb MJ, Chater KF, Kieser T, Bruton CJ, Kieser HM, Lydiate DJ, Smith CP, Ward JM & Schrempf H (1985) Genetic manipulation of Streptomyces: a laboratory manual. Norwich: John Innes Foundation.
Horinouchi S & Beppu T (1992) Autoregulatory factors and communication in actinomycetes. Annu Rev Microbiol. 46: 377–398
Horinouchi S (1996) Streptomyces genes involved in aerial mycelium formation. FEMS Microbiol Lett. 141: 1–9
Janssen GR & Bibb MJ (1993) Derivatives of pUC18 that have BglII sites flanking a modified multiple cloning site and that retain the ability to identify recombinant clones by visual screening of Escherichia coli colonies. Gene 124: 133–134
Khokhlov AS (1991) Microbial Autoregulators. Harwood Academic Publishers, Chur-Reading-Paris-Philadelphia-Tokyo-Melbourne.
Kudo N, Kimura M, Beppu T & Horinouchi S (1995) Cloning and characterization of a gene involved in aerial mycelium formation in Streptomyces griseus. J. Bacteriol. 177: 6401–6410
Larson JL & Herschberger CL (1986) The minimal replicon of a streptomycete plasmid produces an ultrahigh level of plasmid DNA. Plasmid 15: 199–209
MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH & MacNeil T (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilising a novel integration vector. Gene 111: 1–68
Messing J, Crea R & Seeburg PH (1981) A system for shotgun DNA sequencing. Nucleic Acids Res. 9: 309–321
Murray MG (1986) Use of sodium trichloroacetate and mung bean nuclease to increase sensitivity and precision during transcript mapping. Anal. Biochem. 158: 165–170
Narva KE & Feitelson JS (1990) Nucleotide sequence and transcriptional analysis of the redD locus of Streptomyces coelicolor A3(2). J. Bacteriol. 172: 326–333
Strauch E, Takano E, Baylis HA & Bibb MJ (1991) The stringent response in Streptomyces coelicolor A3(2). Mol. Microbiol. 5: 289–298
Strohl WR (1992) Compilation and analysis of DNA sequences associated with apparent streptomycete promoters. Nucleic Acids Res. 20(5): 961–974
Strohl WR (1997) Industrial antibiotics: Today and the future. In: Strohl, WR (Ed) Biotechnology of antibiotics (pp. 1–47). Marcel Dekker, Inc., New York-Basel-Hong Kong.
Szabó G, Vályi-Nagy T & Vitális S (1962) A new factor regulating life cycle of Streptomyces griseus. In: Timakova VD (Ed) Genetics ofMicroorganisms, Proceedings of a Symposium on Heredity and Variability of Microorganisms. State Publishing House on Medical Literature, Moscow.
Szabó PT, Kele Z, Birkó Zs, Szeszák, F, Biró S & Janáky T (1999) Identification of factor C protein from Streptomyces griseus by microelectrospray mass spectrometry. J. Mass Spectrometry 34: 1312–1316
Szeszák F, Vitális S & Szabó G (1991) Presence of factor C in streptomycetes and other bacteria. In: Baumberg S, Krügel H & Noack D (Eds) Genetics and product formation in Streptomyces. Plenum Press, New York-London.
Ueda K, Miyake K, Horinouchi S & Beppu T (1993) A gene cluster involved in aerial mycelium formation in Streptomyces griseus encodes proteins similar to the response regulators of two-component regulatory systems and membrane translocators. J. Bacteriol. 175: 2006–2016
Vara J, Lewandowska-Skarbek M, Wang Y-G, Donadio S & Hutchinson CR (1989) Cloning of genes governing the deoxysugar portion of the erythromycin biosynthesis pathway in Saccharopolyspora erythraea (Streptomyces erythreus). J. Bacteriol. 171: 5872–5881
Vitális S, Szabó G & Vályi-Nagy T (1963) Comparison of streptomycin-producing and non-producing strains of Streptomyces griseus. Acta Biol. Acad. Sci. Hung. 14: 1–15
Vitális S & Szabó G (1969) Cytomorphological effect of factor C in submerged cultures on the hyphae of Streptomyces griseus strain No. 52–1. Acta Biol. Acad. Sci. Hung. 20: 85–92
van Wezel GP,White J, Hoogvliet G & Bibb MJ (2000) Application of redD, the transcriptional activator gene of the undecylprodigiosin biosynthetic pathway, as a reporter for transcriptional activity in Streptomyces coelicolor A3(2) and Streptomyces lividans. J Mol. Microbiol. Biotechnol (In press).
Yamada Y, Nihira T & Sakuda S (1997) Butyrolactone autoregulators, inducers of virginiamycin in Streptomyces virginiae: Their structures, biosynthesis, receptor proteins, and induction of virginiamycin biosynthesis. In: Strohl, WR (Ed) Biotechnology of antibiotics (pp. 63–79). Marcel Dekker, Inc., New York-Basel-Hong Kong.
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Biró, S., Birkó, Z. & van Wezel, G.P. Transcriptional and functional analysis of the gene for factor C, an extracellular signal protein involved in cytodifferentiation of Streptomyces griseus . Antonie Van Leeuwenhoek 78, 277–285 (2000). https://doi.org/10.1023/A:1010221407340
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DOI: https://doi.org/10.1023/A:1010221407340