Skip to main content
NCBI home page
Journal of Bacteriology logoLink to Journal of Bacteriology
. 1990 Oct;172(10):6035–6041. doi: 10.1128/jb.172.10.6035-6041.1990

DNA sequence of the purC gene encoding 5'-phosphoribosyl-5-aminoimidazole-4-N-succinocarboxamide synthetase and organization of the dapA-purC region of Escherichia coli K-12.

A A Tiedeman 1, D J DeMarini 1, J Parker 1, J M Smith 1
PMCID: PMC526926  PMID: 2120198

Abstract

5'-Phosphoribosyl-5-aminoimidazole-4-N-succinocarboxamide synthetase (EC 6.3.2.6), encoded by the purC gene of Escherichia coli K-12, catalyzes the synthesis of 5'-phosphoribosyl-5-aminoimidazole-4-N-succinocarboxamide from 5'-phosphoribosyl-5-aminoimidazole-4-carboxylic acid. The mature protein, as deduced from the purC structural gene sequence, contains 237 amino acids and has a calculated Mr of 26,998. The control region of the purC gene was identified by primer extension mapping of the 5' end of the purC mRNA. The purC control region contains a binding site for and is regulated by the purine repressor, the product of the purR gene. An unusual feature of the 5' untranslated region of the purC mRNA is the presence of a repetitive extragenic palindrome sequence normally found in intercistronic or 3' untranslated regions. The DNA sequence was extended 1.281 kilobases upstream of the purC structural gene and overlapped with the previously determined dapA sequence. Termination of transcription from the dapA-purC intercistronic region may occur within the -35 region of the purC control region. The purC gene has been positioned on the E. coli restriction map and is transcribed in a counterclockwise direction.

Full text

PDF
6035

Images in this article

6038Image
on p.6038

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aiba A., Mizobuchi K. Nucleotide sequence analysis of genes purH and purD involved in the de novo purine nucleotide biosynthesis of Escherichia coli. J Biol Chem. 1989 Dec 15;264(35):21239–21246. [PubMed] [Google Scholar]
  2. Amuro N., Paluh J. L., Zalkin H. Replacement by site-directed mutagenesis indicates a role for histidine 170 in the glutamine amide transfer function of anthranilate synthase. J Biol Chem. 1985 Nov 25;260(27):14844–14849. [PubMed] [Google Scholar]
  3. Andersen L., Kilstrup M., Neuhard J. Pyrimidine, purine and nitrogen control of cytosine deaminase synthesis in Escherichia coli K 12. Involvement of the glnLG and purR genes in the regulation of codA expression. Arch Microbiol. 1989;152(2):115–118. doi: 10.1007/BF00456087. [DOI] [PubMed] [Google Scholar]
  4. Bachmann B. J. Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983 Jun;47(2):180–230. doi: 10.1128/mr.47.2.180-230.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Choi K. Y., Zalkin H. Regulation of Escherichia coli pyrC by the purine regulon repressor protein. J Bacteriol. 1990 Jun;172(6):3201–3207. doi: 10.1128/jb.172.6.3201-3207.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Clarke L., Carbon J. A colony bank containing synthetic Col El hybrid plasmids representative of the entire E. coli genome. Cell. 1976 Sep;9(1):91–99. doi: 10.1016/0092-8674(76)90055-6. [DOI] [PubMed] [Google Scholar]
  7. Dagert M., Ehrlich S. D. Prolonged incubation in calcium chloride improves the competence of Escherichia coli cells. Gene. 1979 May;6(1):23–28. doi: 10.1016/0378-1119(79)90082-9. [DOI] [PubMed] [Google Scholar]
  8. Ebbole D. J., Zalkin H. Cloning and characterization of a 12-gene cluster from Bacillus subtilis encoding nine enzymes for de novo purine nucleotide synthesis. J Biol Chem. 1987 Jun 15;262(17):8274–8287. [PubMed] [Google Scholar]
  9. Fickett J. W. Recognition of protein coding regions in DNA sequences. Nucleic Acids Res. 1982 Sep 11;10(17):5303–5318. doi: 10.1093/nar/10.17.5303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Flannigan K. A., Hennigan S. H., Vogelbacker H. H., Gots J. S., Smith J. M. Purine biosynthesis in Escherichia coli K12: structure and DNA sequence studies of the purHD locus. Mol Microbiol. 1990 Mar;4(3):381–392. doi: 10.1111/j.1365-2958.1990.tb00605.x. [DOI] [PubMed] [Google Scholar]
  11. Gilson E., Perrin D., Clement J. M., Szmelcman S., Dassa E., Hofnung M. Palindromic units from E. coli as binding sites for a chromoid-associated protein. FEBS Lett. 1986 Oct 6;206(2):323–328. doi: 10.1016/0014-5793(86)81005-5. [DOI] [PubMed] [Google Scholar]
  12. Gots J. S., Benson C. E., Jochimsen B., Koduri K. R. Microbial models and regulatory elements in the control of purine metabolism. Ciba Found Symp. 1977;(48):23–41. doi: 10.1002/9780470720301.ch3. [DOI] [PubMed] [Google Scholar]
  13. Harley C. B., Reynolds R. P. Analysis of E. coli promoter sequences. Nucleic Acids Res. 1987 Mar 11;15(5):2343–2361. doi: 10.1093/nar/15.5.2343. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. He B., Shiau A., Choi K. Y., Zalkin H., Smith J. M. Genes of the Escherichia coli pur regulon are negatively controlled by a repressor-operator interaction. J Bacteriol. 1990 Aug;172(8):4555–4562. doi: 10.1128/jb.172.8.4555-4562.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Higgins C. F., Gallagher M. P., Mimmack M. L., Pearce S. R. A family of closely related ATP-binding subunits from prokaryotic and eukaryotic cells. Bioessays. 1988 Apr;8(4):111–116. doi: 10.1002/bies.950080406. [DOI] [PubMed] [Google Scholar]
  16. Hu M. C., Davidson N. Mapping transcription start points on cloned genomic DNA with T4 DNA polymerase: a precise and convenient technique. Gene. 1986;42(1):21–29. doi: 10.1016/0378-1119(86)90146-0. [DOI] [PubMed] [Google Scholar]
  17. Jacobson A. B., Good L., Simonetti J., Zuker M. Some simple computational methods to improve the folding of large RNAs. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):45–52. doi: 10.1093/nar/12.1part1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Kilstrup M., Meng L. M., Neuhard J., Nygaard P. Genetic evidence for a repressor of synthesis of cytosine deaminase and purine biosynthesis enzymes in Escherichia coli. J Bacteriol. 1989 Apr;171(4):2124–2127. doi: 10.1128/jb.171.4.2124-2127.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kohara Y., Akiyama K., Isono K. 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. 1987 Jul 31;50(3):495–508. doi: 10.1016/0092-8674(87)90503-4. [DOI] [PubMed] [Google Scholar]
  20. LUKENS L. N., BUCHANAN J. M. Biosynthesis of the purines. XXIII. The enzymatic synthesis of N-(5-amino-1-ribosyl-4-imidazolylcarbonyl)-L-aspartic acid 5'-phosphate. J Biol Chem. 1959 Jul;234(7):1791–1798. [PubMed] [Google Scholar]
  21. Lin-Chao S., Bremer H. Effect of the bacterial growth rate on replication control of plasmid pBR322 in Escherichia coli. Mol Gen Genet. 1986 Apr;203(1):143–149. doi: 10.1007/BF00330395. [DOI] [PubMed] [Google Scholar]
  22. MILLER R. W., BUCHANAN J. M. Biosynthesis of the purines. 27. N-(5-Amino-1-ribosyl-4-imidazolylcarbonyl)-L-aspartic acid 5'-phosphate kinosynthetase. J Biol Chem. 1962 Feb;237:485–490. [PubMed] [Google Scholar]
  23. Makaroff C. A., Zalkin H. Regulation of Escherichia coli purF. Analysis of the control region of a pur regulon gene. J Biol Chem. 1985 Aug 25;260(18):10378–10387. [PubMed] [Google Scholar]
  24. Martinez H. M. A flexible multiple sequence alignment program. Nucleic Acids Res. 1988 Mar 11;16(5):1683–1691. doi: 10.1093/nar/16.5.1683. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Meng L. M., Kilstrup M., Nygaard P. Autoregulation of PurR repressor synthesis and involvement of purR in the regulation of purB, purC, purL, purMN and guaBA expression in Escherichia coli. Eur J Biochem. 1990 Jan 26;187(2):373–379. doi: 10.1111/j.1432-1033.1990.tb15314.x. [DOI] [PubMed] [Google Scholar]
  26. Merino E., Becerril B., Valle F., Bolivar F. Deletion of a repetitive extragenic palindromic (REP) sequence downstream from the structural gene of Escherichia coli glutamate dehydrogenase affects the stability of its mRNA. Gene. 1987;58(2-3):305–309. doi: 10.1016/0378-1119(87)90386-6. [DOI] [PubMed] [Google Scholar]
  27. Messing J. New M13 vectors for cloning. Methods Enzymol. 1983;101:20–78. doi: 10.1016/0076-6879(83)01005-8. [DOI] [PubMed] [Google Scholar]
  28. Millar G., Lewendon A., Hunter M. G., Coggins J. R. The cloning and expression of the aroL gene from Escherichia coli K12. Purification and complete amino acid sequence of shikimate kinase II, the aroL-gene product. Biochem J. 1986 Jul 15;237(2):427–437. doi: 10.1042/bj2370427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Neidhardt F. C., Bloch P. L., Smith D. F. Culture medium for enterobacteria. J Bacteriol. 1974 Sep;119(3):736–747. doi: 10.1128/jb.119.3.736-747.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Newbury S. F., Smith N. H., Robinson E. C., Hiles I. D., Higgins C. F. Stabilization of translationally active mRNA by prokaryotic REP sequences. Cell. 1987 Jan 30;48(2):297–310. doi: 10.1016/0092-8674(87)90433-8. [DOI] [PubMed] [Google Scholar]
  31. Parker J. Identification of the purC gene product of Escherichia coli. J Bacteriol. 1984 Mar;157(3):712–717. doi: 10.1128/jb.157.3.712-717.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Patey C. A., Shaw G. Purification and properties of an enzyme duet, phosphoribosylaminoimidazole carboxylase and phosphoribosylaminoimidazolesuccinocarboxamide synthetase, involved in the biosynthesis of purine nucleotides de novo. Biochem J. 1973 Nov;135(3):543–545. doi: 10.1042/bj1350543. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Pearson W. R., Lipman D. J. Improved tools for biological sequence comparison. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2444–2448. doi: 10.1073/pnas.85.8.2444. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Richaud F., Richaud C., Ratet P., Patte J. C. Chromosomal location and nucleotide sequence of the Escherichia coli dapA gene. J Bacteriol. 1986 Apr;166(1):297–300. doi: 10.1128/jb.166.1.297-300.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Rolfes R. J., Zalkin H. Escherichia coli gene purR encoding a repressor protein for purine nucleotide synthesis. Cloning, nucleotide sequence, and interaction with the purF operator. J Biol Chem. 1988 Dec 25;263(36):19653–19661. [PubMed] [Google Scholar]
  36. Rolfes R. J., Zalkin H. Regulation of Escherichia coli purF. Mutations that define the promoter, operator, and purine repressor gene. J Biol Chem. 1988 Dec 25;263(36):19649–19652. [PubMed] [Google Scholar]
  37. Sampei G., Mizobuchi K. The organization of the purL gene encoding 5'-phosphoribosylformylglycinamide amidotransferase of Escherichia coli. J Biol Chem. 1989 Dec 15;264(35):21230–21238. [PubMed] [Google Scholar]
  38. Schendel F. J., Mueller E., Stubbe J., Shiau A., Smith J. M. Formylglycinamide ribonucleotide synthetase from Escherichia coli: cloning, sequencing, overproduction, isolation, and characterization. Biochemistry. 1989 Mar 21;28(6):2459–2471. doi: 10.1021/bi00432a017. [DOI] [PubMed] [Google Scholar]
  39. Shiau A., Smith J. M. Improved cat gene cassette for promoter analysis and genetic constructions. Gene. 1988 Jul 30;67(2):295–299. doi: 10.1016/0378-1119(88)90406-4. [DOI] [PubMed] [Google Scholar]
  40. Shine J., Dalgarno L. The 3'-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites. Proc Natl Acad Sci U S A. 1974 Apr;71(4):1342–1346. doi: 10.1073/pnas.71.4.1342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Smith J. M., Daum H. A., 3rd Nucleotide sequence of the purM gene encoding 5'-phosphoribosyl-5-aminoimidazole synthetase of Escherichia coli K12. J Biol Chem. 1986 Aug 15;261(23):10632–10636. [PubMed] [Google Scholar]
  42. Stayton M. M., Rudolph F. B., Fromm H. J. Regulation, genetics, and properties of adenylosuccinate synthetase: a review. Curr Top Cell Regul. 1983;22:103–141. doi: 10.1016/b978-0-12-152822-5.50008-7. [DOI] [PubMed] [Google Scholar]
  43. Tiedeman A. A., Keyhani J., Kamholz J., Daum H. A., 3rd, Gots J. S., Smith J. M. Nucleotide sequence analysis of the purEK operon encoding 5'-phosphoribosyl-5-aminoimidazole carboxylase of Escherichia coli K-12. J Bacteriol. 1989 Jan;171(1):205–212. doi: 10.1128/jb.171.1.205-212.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Tiedeman A. A., Smith J. M., Zalkin H. Nucleotide sequence of the guaA gene encoding GMP synthetase of Escherichia coli K12. J Biol Chem. 1985 Jul 25;260(15):8676–8679. [PubMed] [Google Scholar]
  45. Vieira J., Messing J. Production of single-stranded plasmid DNA. Methods Enzymol. 1987;153:3–11. doi: 10.1016/0076-6879(87)53044-0. [DOI] [PubMed] [Google Scholar]
  46. Watanabe W., Sampei G., Aiba A., Mizobuchi K. Identification and sequence analysis of Escherichia coli purE and purK genes encoding 5'-phosphoribosyl-5-amino-4-imidazole carboxylase for de novo purine biosynthesis. J Bacteriol. 1989 Jan;171(1):198–204. doi: 10.1128/jb.171.1.198-204.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Winans S. C., Elledge S. J., Krueger J. H., Walker G. C. Site-directed insertion and deletion mutagenesis with cloned fragments in Escherichia coli. J Bacteriol. 1985 Mar;161(3):1219–1221. doi: 10.1128/jb.161.3.1219-1221.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Yang Y., Ames G. F. DNA gyrase binds to the family of prokaryotic repetitive extragenic palindromic sequences. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8850–8854. doi: 10.1073/pnas.85.23.8850. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. 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]

Articles from Journal of Bacteriology are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES