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. 1997 Dec;179(24):7784–7789. doi: 10.1128/jb.179.24.7784-7789.1997

A glgC gene essential only for the first of two spatially distinct phases of glycogen synthesis in Streptomyces coelicolor A3(2).

M C Martin 1, D Schneider 1, C J Bruton 1, K F Chater 1, C Hardisson 1
PMCID: PMC179742  PMID: 9401038

Abstract

By using a PCR approach based on conserved regions of ADP-glucose pyrophosphorylases, a glgC gene was cloned from Streptomyces coelicolor A3(2). The deduced glgC gene product showed end-to-end relatedness to other bacterial ADP-glucose pyrophosphorylases. The glgC gene is about 1,000 kb from the leftmost chromosome end and is not closely linked to either of the two glgB genes of S. coelicolor, which encode glycogen branching enzymes active in different locations in differentiated colonies. Disruption of glgC eliminated only the first of two temporal peaks of ADP-glucose pyrophosphorylase activity and glycogen accumulation and prevented cytologically observable glycogen accumulation in the substrate mycelium of colonies (phase I), while glycogen deposition in young spore chains (phase II) remained readily detectable. The cloned glgC gene therefore encodes an ADP-glucose pyrophosphorylase essential only for phase I (and it is therefore named glgCI). A second, phase II-specific, glgC gene should also exist in S. coelicolor, though it was not detected by hybridization analysis.

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Selected References

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  1. Bibb M. J., Findlay P. R., Johnson M. W. The relationship between base composition and codon usage in bacterial genes and its use for the simple and reliable identification of protein-coding sequences. Gene. 1984 Oct;30(1-3):157–166. doi: 10.1016/0378-1119(84)90116-1. [DOI] [PubMed] [Google Scholar]
  2. Birnboim H. C., Doly J. A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979 Nov 24;7(6):1513–1523. doi: 10.1093/nar/7.6.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. Braña A. F., Manzanal M. B., Hardisson C. Characterization of intracellular polysaccharides of Streptomyces. Can J Microbiol. 1982 Dec;28(12):1320–1323. doi: 10.1139/m82-197. [DOI] [PubMed] [Google Scholar]
  5. Braña A. F., Manzanal M. B., Hardisson C. Occurrence of polysaccharide granules in sporulating hyphae of Streptomyces viridochromogenes. J Bacteriol. 1980 Dec;144(3):1139–1142. doi: 10.1128/jb.144.3.1139-1142.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Braña A. F., Méndez C., Díaz L. A., Manzanal M. B., Hardisson C. Glycogen and trehalose accumulation during colony development in Streptomyces antibioticus. J Gen Microbiol. 1986 May;132(5):1319–1326. doi: 10.1099/00221287-132-5-1319. [DOI] [PubMed] [Google Scholar]
  7. Bruton C. J., Guthrie E. P., Chater K. F. Phage vectors that allow monitoring of transcription of secondary metabolism genes in Streptomyces. Biotechnology (N Y) 1991 Jul;9(7):652–656. doi: 10.1038/nbt0791-652. [DOI] [PubMed] [Google Scholar]
  8. Bruton C. J., Plaskitt K. A., Chater K. F. Tissue-specific glycogen branching isoenzymes in a multicellular prokaryote, Streptomyces coelicolor A3(2). Mol Microbiol. 1995 Oct;18(1):89–99. doi: 10.1111/j.1365-2958.1995.mmi_18010089.x. [DOI] [PubMed] [Google Scholar]
  9. Burton R. A., Bewley J. D., Smith A. M., Bhattacharyya M. K., Tatge H., Ring S., Bull V., Hamilton W. D., Martin C. Starch branching enzymes belonging to distinct enzyme families are differentially expressed during pea embryo development. Plant J. 1995 Jan;7(1):3–15. doi: 10.1046/j.1365-313x.1995.07010003.x. [DOI] [PubMed] [Google Scholar]
  10. Chater K. F., Bruton C. J., King A. A., Suarez J. E. The expression of Streptomyces and Escherichia coli drug-resistance determinants cloned into the Streptomyces phage phi C31. Gene. 1982 Jul-Aug;19(1):21–32. doi: 10.1016/0378-1119(82)90185-8. [DOI] [PubMed] [Google Scholar]
  11. Chater K. F. Multilevel regulation of Streptomyces differentiation. Trends Genet. 1989 Nov;5(11):372–377. doi: 10.1016/0168-9525(89)90172-8. [DOI] [PubMed] [Google Scholar]
  12. Hardisson C., Manzanal M. B., Salas J. A., Suárez J. E. Fine structure, physiology and biochemistry of arthrospore germination in Streptomyces antibioticus. J Gen Microbiol. 1978 Apr;105(2):203–214. doi: 10.1099/00221287-105-2-203. [DOI] [PubMed] [Google Scholar]
  13. Hardisson C., Manzanal M. B. Ultrastructural studies of sporulation in Streptomyces. J Bacteriol. 1976 Sep;127(3):1443–1454. doi: 10.1128/jb.127.3.1443-1454.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Henikoff S. Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene. 1984 Jun;28(3):351–359. doi: 10.1016/0378-1119(84)90153-7. [DOI] [PubMed] [Google Scholar]
  15. Hill M. A., Kaufmann K., Otero J., Preiss J. Biosynthesis of bacterial glycogen. Mutagenesis of a catalytic site residue of ADP-glucose pyrophosphorylase from Escherichia coli. J Biol Chem. 1991 Jul 5;266(19):12455–12460. [PubMed] [Google Scholar]
  16. Ikeda H., Seno E. T., Bruton C. J., Chater K. F. Genetic mapping, cloning and physiological aspects of the glucose kinase gene of Streptomyces coelicolor. Mol Gen Genet. 1984;196(3):501–507. doi: 10.1007/BF00436199. [DOI] [PubMed] [Google Scholar]
  17. Janssen G. R., Bibb M. J. 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. 1993 Feb 14;124(1):133–134. doi: 10.1016/0378-1119(93)90774-w. [DOI] [PubMed] [Google Scholar]
  18. Kiel J. A., Boels J. M., Beldman G., Venema G. Glycogen in Bacillus subtilis: molecular characterization of an operon encoding enzymes involved in glycogen biosynthesis and degradation. Mol Microbiol. 1994 Jan;11(1):203–218. doi: 10.1111/j.1365-2958.1994.tb00301.x. [DOI] [PubMed] [Google Scholar]
  19. Kieser H. M., Kieser T., Hopwood D. A. A combined genetic and physical map of the Streptomyces coelicolor A3(2) chromosome. J Bacteriol. 1992 Sep;174(17):5496–5507. doi: 10.1128/jb.174.17.5496-5507.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kieser T., Hopwood D. A. Genetic manipulation of Streptomyces: integrating vectors and gene replacement. Methods Enzymol. 1991;204:430–458. doi: 10.1016/0076-6879(91)04023-h. [DOI] [PubMed] [Google Scholar]
  21. Larsen C. E., Lee Y. M., Preiss J. Covalent modification of the inhibitor-binding site(s) of Escherichia coli ADP-glucose synthetase. Isolation and structural characterization of 8-azido-AMP-incorporated peptides. J Biol Chem. 1986 Nov 25;261(33):15402–15409. [PubMed] [Google Scholar]
  22. Lee Y. M., Preiss J. Covalent modification of substrate-binding sites of Escherichia coli ADP-glucose synthetase. Isolation and structural characterization of 8-azido-ADP-glucose-incorporated peptides. J Biol Chem. 1986 Jan 25;261(3):1058–1064. [PubMed] [Google Scholar]
  23. Liu M. Y., Yang H., Romeo T. The product of the pleiotropic Escherichia coli gene csrA modulates glycogen biosynthesis via effects on mRNA stability. J Bacteriol. 1995 May;177(10):2663–2672. doi: 10.1128/jb.177.10.2663-2672.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Loewen P. C., Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol. 1994;48:53–80. doi: 10.1146/annurev.mi.48.100194.000413. [DOI] [PubMed] [Google Scholar]
  25. Lomovskaya N. D., Mkrtumian N. M., Gostimskaya N. L., Danilenko V. N. Characterization of temperate actinophage phi C31 isolated from Streptomyces coelicolor A3(2). J Virol. 1972 Feb;9(2):258–262. doi: 10.1128/jvi.9.2.258-262.1972. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. MacNeil D. J., Gewain K. M., Ruby C. L., Dezeny G., Gibbons P. H., MacNeil T. Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene. 1992 Feb 1;111(1):61–68. doi: 10.1016/0378-1119(92)90603-m. [DOI] [PubMed] [Google Scholar]
  27. Manzanal M. B., Hardisson C. Early stages of arthrospore maturation in Streptomyces. J Bacteriol. 1978 Jan;133(1):293–297. doi: 10.1128/jb.133.1.293-297.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. McVittie A. Ultrastructural studies on sporulation in wild-type and white colony mutants of Streptomyces coelicolor. J Gen Microbiol. 1974 Apr;81(2):291–302. doi: 10.1099/00221287-81-2-291. [DOI] [PubMed] [Google Scholar]
  29. Mizusawa S., Nishimura S., Seela F. Improvement of the dideoxy chain termination method of DNA sequencing by use of deoxy-7-deazaguanosine triphosphate in place of dGTP. Nucleic Acids Res. 1986 Feb 11;14(3):1319–1324. doi: 10.1093/nar/14.3.1319. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Murray N. E., Brammar W. J., Murray K. Lambdoid phages that simplify the recovery of in vitro recombinants. Mol Gen Genet. 1977 Jan 7;150(1):53–61. doi: 10.1007/BF02425325. [DOI] [PubMed] [Google Scholar]
  31. Olukoshi E. R., Packter N. M. Importance of stored triacylglycerols in Streptomyces: possible carbon source for antibiotics. Microbiology. 1994 Apr;140(Pt 4):931–943. doi: 10.1099/00221287-140-4-931. [DOI] [PubMed] [Google Scholar]
  32. Parsons T. F., Preiss J. Biosynthesis of bacterial glycogen. Isolation and characterization of the pyridoxal-P allosteric activator site and the ADP-glucose-protected pyridoxal-P binding site of Escherichia coli B ADP-glucose synthase. J Biol Chem. 1978 Nov 10;253(21):7638–7645. [PubMed] [Google Scholar]
  33. Preiss J., Crawford K., Downey J., Lammel C., Greenberg E. Kinetic properties of Serratia marcescens adenosine 5'-diphosphate glucose pyrophosphorylase. J Bacteriol. 1976 Jul;127(1):193–203. doi: 10.1128/jb.127.1.193-203.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Preiss J., Romeo T. Physiology, biochemistry and genetics of bacterial glycogen synthesis. Adv Microb Physiol. 1989;30:183–238. doi: 10.1016/s0065-2911(08)60113-7. [DOI] [PubMed] [Google Scholar]
  35. Redenbach M., Kieser H. M., Denapaite D., Eichner A., Cullum J., Kinashi H., Hopwood D. A. A set of ordered cosmids and a detailed genetic and physical map for the 8 Mb Streptomyces coelicolor A3(2) chromosome. Mol Microbiol. 1996 Jul;21(1):77–96. doi: 10.1046/j.1365-2958.1996.6191336.x. [DOI] [PubMed] [Google Scholar]
  36. Richardson M. A., Kuhstoss S., Solenberg P., Schaus N. A., Rao R. N. A new shuttle cosmid vector, pKC505, for streptomycetes: its use in the cloning of three different spiramycin-resistance genes from a Streptomyces ambofaciens library. Gene. 1987;61(3):231–241. doi: 10.1016/0378-1119(87)90187-9. [DOI] [PubMed] [Google Scholar]
  37. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Schneider D., Bruton C. J., Chater K. F. Characterization of spaA, a Streptomyces coelicolor gene homologous to a gene involved in sensing starvation in Escherichia coli. Gene. 1996 Oct 24;177(1-2):243–251. doi: 10.1016/0378-1119(96)00310-1. [DOI] [PubMed] [Google Scholar]
  39. Smith-White B. J., Preiss J. Comparison of proteins of ADP-glucose pyrophosphorylase from diverse sources. J Mol Evol. 1992 May;34(5):449–464. doi: 10.1007/BF00162999. [DOI] [PubMed] [Google Scholar]
  40. Wildermuth H., Hopwood D. A. Septation during sporulation in Streptomyces coelicolor. J Gen Microbiol. 1970 Jan;60(1):51–59. doi: 10.1099/00221287-60-1-51. [DOI] [PubMed] [Google Scholar]
  41. Yang H., Liu M. Y., Romeo T. Coordinate genetic regulation of glycogen catabolism and biosynthesis in Escherichia coli via the CsrA gene product. J Bacteriol. 1996 Feb;178(4):1012–1017. doi: 10.1128/jb.178.4.1012-1017.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. 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. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  43. Zalacain M., González A., Guerrero M. C., Mattaliano R. J., Malpartida F., Jiménez A. Nucleotide sequence of the hygromycin B phosphotransferase gene from Streptomyces hygroscopicus. Nucleic Acids Res. 1986 Feb 25;14(4):1565–1581. doi: 10.1093/nar/14.4.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]

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