Advertisement

Molecular and General Genetics MGG

, Volume 226, Issue 1–2, pp 321–327 | Cite as

Characterization of two genes, glpQ and ugpQ, encoding glycerophosphoryl diester phosphodiesterases of Escherichia coli

  • Jan Tommassen
  • Karin Eiglmeier
  • Stewart T. Cole
  • Piet Overduin
  • Timothy J. Larson
  • Winfried Boos
Short Communications

Summary

The nucleotide sequences of the glpQ and ugpQ genes of Escherichia coli, which both encode glycerophosphoryl diester phosphodiesterases, were determined. The glpQ gene encodes a periplasmic enzyme of 333 amino acids, produced initially with a 25 residue long signal sequence, while ugpQ codes for a cytoplasmic protein of 247 amino acids. Despite differences in size and cellular location, significant similarity in the primary structures of the two enzymes was found suggesting a common evolutionary origin. The 3′ end of the ugpQ gene overlaps an open reading frame that is transcribed in the opposite direction. This open reading frame encodes a polypeptide with an unusual composition, i.e., 46 of the 146 amino acids are Gln or Asn. This polypeptide and the UgpQ protein were identified in an in vitro transcription/translation system as proteins with apparent molecular weights of 19.5 and 27 kDa, respectively.

Key words

Escherichia coli K12 glpQ gene ugpQ gene Overlapping genes Glycerophosphoryl diester phosphodiesterase 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Ambudkar SV, Larson TJ, Maloney PC (1986) Reconstitution of sugar phosphate transport systems of Escherichia coli. J Biol Chem 261:9083–9086Google Scholar
  2. Argast M, Boos W (1980) Co-regulation in Escherichia coli of a novel transport system for sn-glycerol-3-phosphate and outer membrane protein Ic (e, E) with alkaline phosphatase and phosphate-binding protein. J Bacteriol 143:142–150Google Scholar
  3. Biggin MD, Gibson TJ, Hong GF (1983) Buffer gradient gels and 35S-label s an aid to rapid DNA sequence determination. Proc Natl Acad Sci USA 80:3963–3965Google Scholar
  4. Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523Google Scholar
  5. Brzoska P, Boos W (1988) Characteristics of a ugp-encoded and phoB-dependent glycerophosphoryl diester phosphodiesterase which is physically dependent on the Ugp transport system of Escherichia coli. J Bacteriol 170:4125–4135Google Scholar
  6. Carlson J, Fuchs JA, Messing J (1984) Primary structure of the Escherichia coli ribonucleoside diphosphate reductase operon. Proc Natl Acad Sci USA 81:4294–4297Google Scholar
  7. Cole ST, Eiglmeier K, Ahmed S, Honore N, Elmes L, Anderson WF, Weiner JH (1988) Nucleotide sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K-12. J Bacteriol 170:2448–2456Google Scholar
  8. Cozzarelli NR, Freedberg WB, Lin ECC (1968) Genetic control of the L-α-glycerophosphate system in E. coli. J Mol Biol 31:371–387Google Scholar
  9. Davanloo P, Rosenberg AH, Dunn JJ, Studier FW (1984) Cloning and expression of the gene for bacteriophage T7 RNA polymerase. Proc Natl Acad Sci USA 81:2035–2039Google Scholar
  10. de Vrije T, Tommassen J, de Kruijff B (1987) Optimal posttranslational translocation of the precursor of PhoE protein across Escherichia coli membrane vesicles requires both ATP and the protonmotive force. Biochim Biophys Acta 900:63–72Google Scholar
  11. Eiglmeier K, Boos W, Cole ST (1987) Nucleotide sequence and transcriptional startpoint of the glpT gene of Escherichia coli: extensive sequence homology of the glycerol-3-phosphate transport protein with components of the hexose-6-phosphate transport system. Mol Microbiol 1:251–258Google Scholar
  12. Elvin CM, Hardy CM, Rosenberg H (1985) Pi exchange mediated by the GlpT-dependent sn-glycerol-3-phosphate transport system in Escherichia coli. J Bacteriol 161:1054–1058Google Scholar
  13. Hantke K (1988) Characterization of an iron sensitive Mudl mutant in E. coli lacking the ribonucleotide reductase subunit B2. Arch Microbiol 149:344–349Google Scholar
  14. Kasahara M, Makino K, Amemura M, Nakata A (1989) Nucleotide sequence of the ugpQ gene encoding glycerophosphoryl diester phosphodiesterase of Escherichia coli K-12. Nucleic Acids Res 17:2854Google Scholar
  15. Kohara Y, Akiyama K, Isono K (1987) The physical map of the whole E. coli chromosome: application of a new strategy for rapid analysis and sorting of a large genomic library. Cell 50:495–508Google Scholar
  16. Kolaskar AS, Reddy BVB (1985) A method to locate protein coding sequences in DNA of prokaryotic systems. Nucleic Acids Res 13:185–194Google Scholar
  17. Larson TJ, van Loo-Bhattacharya (1988) Purification and characterization of glpQ-encoded glycerophosphodiester phosphodiesterase from Escherichia coli K-12. Arch Biochem Biophys 260:577–584Google Scholar
  18. Larson TJ, Schumacher G, Boos W (1982) Identification of the glpT-encoded sn-glycerol-3-phosphate permease of Escherichia coli, an oligomeric integral membrane protein. J Bacteriol 152:1008–1021Google Scholar
  19. Larson TJ, Ehrmann M, Boos W (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258:5428–5432Google Scholar
  20. Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1440Google Scholar
  21. Lugtenberg B, Meijers J, Peters R, van der Hoek P, van Alphen L (1975) Electrophoretic resolution of the “major outer membrane protein” of Escherichia coli K12 into four bands. FEBS Lett 58:254–258Google Scholar
  22. Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New YorkGoogle Scholar
  23. Messing J, Crea R, Seeburg PH (1981) A system for shotgun DNA sequencing. Nucleic Acids Res 9:309–321Google Scholar
  24. Okita TW, Cheesbrough V, Reeves CD (1985) Evolution and heterogeneity of the α-/β-type and γ-type gliadin DNA sequences. J Biol Chem 260:8203–8213Google Scholar
  25. Overduin P, Boos W, Tommassen J (1988) Nucleotide sequence of the ugp genes of Escherichia coli K-12: homology to the maltose system. Mol Microbiol 2:767–775Google Scholar
  26. Schryvers A, Weiner JH (1982) The anaerobic sn-glycerol-3-phosphate dehydrogenase: cloning and expression of the glpA gene of Escherichia coli and identification of the glpA products. Can J Biochem 60:224–231Google Scholar
  27. Schweizer H, Boos W (1984) Characterization of the ugp region containing the genes for the phoB dependent sn-glycerol-3-phos-phate transport system of Escherichia coli. Mol Gen Genet 197:161–168Google Scholar
  28. Schweizer H, Grussenmeyer T, Boos W (1982) Mapping of two ugp genes coding for the pho regulon dependent sn-glycerol-3-phosphate transport system of Escherichia coli. J Bacteriol 150:1164–1171Google Scholar
  29. von Heijne G (1984) How signal sequences maintain cleavage specificity. J Mol Biol 173:243–251Google Scholar
  30. von Heijne G (1990) The signal peptide. J Membr Biol 115:195–201Google Scholar
  31. Vyas NK, Vyas MN, Quicho FA (1987) A novel calcium binding site in the galactose-binding protein of bacterial transport and chemotaxis. Nature 327:635–638Google Scholar
  32. Yamada M, Takeda Y, Okamoto K, Hirota Y (1982) Physical map of the nrdA-nrdB-ftsB-glpT region of the chromosomal DNA of E. coli. Gene 18:309–318Google Scholar
  33. Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequence of the Ml3mp18 and pUC19 vectors. Gene 33:113–119Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • Jan Tommassen
    • 1
    • 2
  • Karin Eiglmeier
    • 3
    • 4
  • Stewart T. Cole
    • 4
  • Piet Overduin
    • 1
  • Timothy J. Larson
    • 5
  • Winfried Boos
    • 3
  1. 1.Department of Molecular Cell BiologyUniversity of UtrechtUtrechtThe Netherlands
  2. 2.Institute of Molecular Biology and Medical BiotechnologyUniversity of UtrechtUtrechtThe Netherlands
  3. 3.Department of BiologyUniversity of KonstanzKonstanzGermany
  4. 4.Laboratoire de Génétique Moléculaire BactérienneInstitut PasteurParis Cedex 15France
  5. 5.Department of Biochemistry and NutritionVirginia TechBlacksburgUSA

Personalised recommendations