Advertisement

Antonie van Leeuwenhoek

, Volume 78, Issue 3–4, pp 243–251 | Cite as

Sugar uptake and utilisation in Streptomyces coelicolor: a PTS view to the genome

  • Stephan Parche
  • Harald Nothaft
  • Annette Kamionka
  • Fritz Titgemeyer
Article

Abstract

Our research group is studying the phosphotransferase system (PTS) of Streptomyces coelicolor, which, in other bacteria, is centrally involved in carbon source uptake and regulation. We have surveyed the public available S. coelicolor genome sequence produced by the ongoing genome sequencing project for pts gene homologues (http://www.sanger.ac.uk/Projects/S_coelicolor/). Three genes encoding homologues of the general PTS components enzyme I (ptsI), HPr (ptsH), and enzyme IIACrr (crr; IIAGlc-homologue) and six genes encoding homologues of sugar-specific PTS components were identified. The deduced primary sequences of the sugar-specific components shared significant similarities to PTS permeases of the mannitol/fructose family and of the glucose/sucrose family. A model is presented, in which possible functions of the novel described PTS homologues are discussed.

PTS phosphotransferase system sugar transport Streptomyces 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Alpert CA, Dorschug M, Saffen D, Frank R, Deutscher J & Hengstenberg W (1985) The bacterial phosphoenolpyruvatedependent phosphotransferase system. Isolation of active site peptides by reversed-phase high-performance liquid chromatography and determination of their primary structure. J. Chromatogr. 326: 363–371Google Scholar
  2. Ausubel FA, Brent R, Kingston RE, Moore DD, Seidmann JG, Smith JA & Struhl K(1990) Current protocols in molecular biology. Greene Publishing and Wiley-Interscience, New York.Google Scholar
  3. Bibb M (1996) 1995 Colworth Prize Lecture. The regulation of antibiotic production in Streptomyces coelicolor A3(2). Microbiology 142: 1335–1344Google Scholar
  4. Bouma CL & Roseman S (1996) Sugar transport by the marine chitinolytic bacterium Vibrio furnissii. Molecular cloning and analysis of the glucose and N-acetylglucosamine permeases. J. Biol. Chem. 271: 33457–33467Google Scholar
  5. Butler MJ, Deutscher J, Postma PW, Wilson TJ, Galinier A & Bibb MJ (1999) Analysis of a ptsH homologue from Streptomyces coelicolor A3(2). FEMS Microbiol. Lett. 177: 279–288Google Scholar
  6. Champness WC (1988) New loci required for Streptomyces coelicolor morphological and physiological differentiation. J. Bacteriol. 170: 1168–1174Google Scholar
  7. Chater KF (1998) Taking a genetic scalpel to the Streptomyces colony. Microbiology 144: 1465–1478Google Scholar
  8. Chater KF & Hopwood DA (1983) Streptomyces. In: Sonenshein AL, Hoch JA & Losick R (Eds) Bacillus subtilis and other Gram-positive bacteria (pp 83–99). American Society for Microbiology, Washington DC.Google Scholar
  9. Christiansen I & Hengstenberg W (1999) Staphylococcal phosphoenolpyruvate-dependent phosphotransferase system-two highly similar glucose permeases in Staphylococcus carnosus with different glucoside specificity: protein engineering in vivo? Microbiology 145: 2881–2889Google Scholar
  10. Dahl M (1997) Enzyme IIGlc contributes to trehalose metabolism in Bacillus subtilis. FEMS Microbiol. Lett. 148: 233–238Google Scholar
  11. Hengstenberg W, Penberthy WK, Hill KL & Morse ML (1969) Phosphotransferase system of Staphylococcus aureus: its requirement for the accumulation and metabolism of galactosides. J. Bacteriol. 99: 383–388Google Scholar
  12. Hopwood DA (1999) Forty years of genetics with Streptomyces: from in vivo through in vitro to in silico. Microbiology 145: 2183–2202Google Scholar
  13. 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. John Innes Foundation, Norwich.Google Scholar
  14. Hopwood DA, Chater KF & Bibb MJ (1995) Genetics of antibiotic production in Streptomyces coelicolor A3(2), a model streptomycete. Biotechnology 28: 65–102Google Scholar
  15. Macfadyen LP, Dorocicz IR, Reizer J, Saier MH, Jr. & Redfield RJ (1996) Regulation of competence development and sugar utilization in Haemophilus influenzae Rd by a phosphoenolpyruvate: fructose phosphotransferase system. Mol. Microbiol. 21: 941–952.Google Scholar
  16. MacNeil DJ, Gewain KM, Ruby CL, Dezeny G, Gibbons PH & MacNeil T (1992) Analysis of Streptomyces avermitilis genes required for avermectin biosynthesis utilizing a novel integration vector. Gene 111: 61–68Google Scholar
  17. Marck C (1988) 'DNA Strider': a 'C' program for the fast analysis of DNA and protein sequences on the Apple Macintosh family of computers. Nucleic Acids Res. 16: 1829–1836Google Scholar
  18. Merrick MJ (1976) A morphological and genetic mapping study of bald colony mutants of Streptomyces coelicolor. J. Gen. Microbiol. 96: 299–315Google Scholar
  19. Ni X & Westpheling J (1997) Direct repeat sequences in the Streptomyces chitinase-63 promoter direct both glucose repression and chitin induction. Proc. Natl. Acad. Sci. USA 94: 13116–13121Google Scholar
  20. Oh SH & Chater KF (1997) Denaturation of circular or linear DNA facilitates targeted integrative transformation of Streptomyces coelicolor A3(2): possible relevance to other organisms. J. Bacteriol. 179: 122–127Google Scholar
  21. Orchard LM & Kornberg HL (1990) Sequence similarities between the gene specifying 1–phosphofructokinase (fruK), genes specifying other kinases in Escherichia coli K12, and lacC of Staphylococcus aureus. Proc. R. Soc. Lond. B Biol. Sci. 242: 87–90Google Scholar
  22. Parche S, Schmid R & Titgemeyer F (1999) The phosphotransferase system (PTS) of Streptomyces coelicolor: identification and biochemical analysis of a histidine phosphocarrier protein HPr encoded by the gene ptsH. Eur. J. Biochem. 265: 308–317Google Scholar
  23. Poolman B, Knol J, Mollet B, Nieuwenhuis B & Sulter G (1995) Regulation of bacterial sugar-H+ symport by phosphoenolpyruvate-dependent enzyme I/HPr-mediated phosphorylation. Proc. Natl. Acad. Sci. USA 92: 778–782Google Scholar
  24. Pope MK, Green BD & Westpheling J (1996) The bld mutants of Streptomyces coelicolor are defective in the regulation of carbon utilization, morphogenesis and cell-cell signalling. Mol. Microbiol. 19: 747–756Google Scholar
  25. Postma PW, Lengeler JW & Jacobson GR (1993) Phosphoenolpyruvate: carbohydrate phosphotransferase systems of bacteria. Microbiol. Rev. 57: 543–594Google Scholar
  26. Presper KA, Wong CY, Liu L, Meadow ND & Roseman S (1989) Site-directed mutagenesis of the phosphocarrier protein. IIIGlc, a major signal-transducing protein in Escherichia coli. Proc. Natl. Acad. Sci. USA 86: 4052–4055Google Scholar
  27. Reidl J & Boos W (1991) The malX malY operon of Escherichia coli encodes a novel enzyme II of the phosphotransferase system recognizing glucose and maltose and an enzyme abolishing the endogenous induction of the maltose system. J. Bacteriol. 173: 4862–4876Google Scholar
  28. Reizer J, Charbit A, Reizer A & Saier MH, Jr. (1996a) Novel phosphotransferase system genes revealed by bacterial genome analysis: operons encoding homologues of sugar-specific permease domains of the phosphotransferase system and pentose catabolic enzymes. Genome Sci. Technol. 1: 53–75Google Scholar
  29. Reizer J, Paulsen IT, Reizer A, Titgemeyer F & Saier MH, Jr. (1996b) Novel phosphotransferase system genes revealed by bacterial genome analysis: the complete complement of pts genes in Mycoplasma genitalium. Microb. Comp. Genomics 1: 151–164Google Scholar
  30. Reizer J, Reizer A & Saier MH, Jr. (1996c) Novel PTS proteins revealed by bacterial genome sequencing: a unique fructosespecific phosphoryl transfer protein with two HPr-like domains in Haemophilus influenzae. Res. Microbiol. 147: 209–215Google Scholar
  31. Reizer J, Bachem S, Reizer A, Arnaud M, Saier MH, Jr. & Stülke J (1999) Novel phosphotransferase system genes revealed by genome analysis-the complete complement of PTS proteins encoded within the genome of Bacillus subtilis. Microbiology 145: 3419–3429Google Scholar
  32. Saier MH, Jr. (1993) Regulatory interactions involving the proteins of the phosphotransferase system in enteric bacteria. J. Cell. Biochem. 51: 62–68Google Scholar
  33. Saier MH, Jr. & Reizer J (1994) The bacterial phosphotransferase system: new frontiers 30 years later. Mol. Microbiol. 13: 755–764Google Scholar
  34. Saier MH, Jr., Chauvaux S, Cook GM, Deutscher J, Paulsen IT, Reizer J & Ye JJ (1996) Catabolite repression and inducer control in Gram-positive bacteria. Microbiology 142: 217–230Google Scholar
  35. Stülke J & Hillen W(1999) Carbon catabolite repression in bacteria. Curr. Opin. Microbiol. 2: 195–201Google Scholar
  36. Stülke J, Martin-Verstraete I, Charrier V, Klier A, Deutscher J & Rapoport G (1995) The HPr protein of the phosphotransferase system links induction and catabolite repression of the Bacillus subtilis levanase operon. J. Bacteriol. 177: 6928–6936Google Scholar
  37. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F & Higgins DG (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876–4882Google Scholar
  38. Titgemeyer F (1993) Signal transduction in chemotaxis mediated by the bacterial phosphotransferase system. J. Cell. Biochem. 51: 69–74Google Scholar
  39. Titgemeyer F, Mason RE & Saier MH, Jr. (1994a) Regulation of the raffinose permease of Escherichia coli by the glucose-specific enzyme IIA of the phosphoenolpyruvate:sugar phosphotransferase system. J. Bacteriol. 176: 543–546Google Scholar
  40. Titgemeyer F, Walkenhorst J, Cui X, Reizer J & Saier MH, Jr. (1994b) Proteins of the phosphoenolpyruvate:sugar phosphotransferase system in Streptomyces: possible involvement in the regulation of antibiotic production. Res. Microbiol. 145: 89–92Google Scholar
  41. Titgemeyer F, Walkenhorst J, Reizer J, Stuiver MH, Cui X & Saier MH, Jr. (1995) Identification and characterization of phosphoenolpyruvate: fructose phosphotransferase systems in three Streptomyces species. Microbiology 141: 51–58Google Scholar

Copyright information

© Kluwer Academic Publishers 2000

Authors and Affiliations

  • Stephan Parche
    • 1
  • Harald Nothaft
    • 1
  • Annette Kamionka
    • 1
  • Fritz Titgemeyer
    • 2
  1. 1.Lehrstuhl für MikrobiologieFriedrich-Alexander-Universität Erlangen-NürnbergErlangenGermany
  2. 2.Lehrstuhl für MikrobiologieFriedrich-Alexander-Universität Erlangen-NürnbergErlangenGermany

Personalised recommendations