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.
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References
Ambudkar SV, Larson TJ, Maloney PC (1986) Reconstitution of sugar phosphate transport systems of Escherichia coli. J Biol Chem 261:9083–9086
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 143:142–150
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 80:3963–3965
Birnboim HC, Doly J (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res 7:1513–1523
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 170:4125–4135
Carlson J, Fuchs JA, Messing J (1984) Primary structure of the Escherichia coli ribonucleoside diphosphate reductase operon. Proc Natl Acad Sci USA 81:4294–4297
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 170:2448–2456
Cozzarelli NR, Freedberg WB, Lin ECC (1968) Genetic control of the L-α-glycerophosphate system in E. coli. J Mol Biol 31:371–387
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 81:2035–2039
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 900:63–72
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 1:251–258
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 161:1054–1058
Hantke K (1988) Characterization of an iron sensitive Mudl mutant in E. coli lacking the ribonucleotide reductase subunit B2. Arch Microbiol 149:344–349
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 17:2854
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 50:495–508
Kolaskar AS, Reddy BVB (1985) A method to locate protein coding sequences in DNA of prokaryotic systems. Nucleic Acids Res 13:185–194
Larson TJ, van Loo-Bhattacharya (1988) Purification and characterization of glpQ-encoded glycerophosphodiester phosphodiesterase from Escherichia coli K-12. Arch Biochem Biophys 260:577–584
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 152:1008–1021
Larson TJ, Ehrmann M, Boos W (1983) Periplasmic glycerophosphodiester phosphodiesterase of Escherichia coli, a new enzyme of the glp regulon. J Biol Chem 258:5428–5432
Lipman DJ, Pearson WR (1985) Rapid and sensitive protein similarity searches. Science 227:1435–1440
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 58:254–258
Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
Messing J, Crea R, Seeburg PH (1981) A system for shotgun DNA sequencing. Nucleic Acids Res 9:309–321
Okita TW, Cheesbrough V, Reeves CD (1985) Evolution and heterogeneity of the α-/β-type and γ-type gliadin DNA sequences. J Biol Chem 260:8203–8213
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 2:767–775
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 60:224–231
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 197:161–168
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 150:1164–1171
von Heijne G (1984) How signal sequences maintain cleavage specificity. J Mol Biol 173:243–251
von Heijne G (1990) The signal peptide. J Membr Biol 115:195–201
Vyas NK, Vyas MN, Quicho FA (1987) A novel calcium binding site in the galactose-binding protein of bacterial transport and chemotaxis. Nature 327:635–638
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 18:309–318
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 33:113–119
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Communicated by J.W. Lengeler
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Tommassen, J., Eiglmeier, K., Cole, S.T. et al. Characterization of two genes, glpQ and ugpQ, encoding glycerophosphoryl diester phosphodiesterases of Escherichia coli . Mol Gen Genet 226, 321–327 (1991). https://doi.org/10.1007/BF00273621
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DOI: https://doi.org/10.1007/BF00273621