Dra-nupC-pdp Operon of Bacillus Subtilis: Nucleotide Sequence, Induction by Deoxyribonucleosides, and Transcriptional Regulation by the DeoR-encoded DeoR Repressor Protein

Overview

Journal J Bacteriol

Publisher American Society for Microbiology

Specialty Microbiology

Date 1996 Jan 1

PMID 8550462

Citations 37

Authors

H H Saxild

L N Andersen

K Hammer

Affiliations

Soon will be listed here.

Abstract

The genes encoding deoxyriboaldolase (dra), nucleoside uptake protein (nupC), and pyrimidine nucleoside sequences were determined. Sequence analysis showed that the genes were localized immediately downstream of the hut operon. Insertional gene disruption studies indicated that the three genes constitute an operon with the gene order dra-nupC-pdp. A promoter mapping immediately upstream of the dra gene was identified, and downstream of the pdp gene the nucleotide sequence indicated the existence of a factor-independent transcription terminator structure. In wild-type cells growing in succinate minimal medium, the pyrimidine nucleoside phosphorylase and deoxyriboaldolase levels were five- to eightfold higher in the presence of thymidine and fourfold higher in the presence of deoxyadenosine. By the use of lacZ fusions, the regulation was found to be at the level of transcription. The operon expression was subject to glucose repression. Upstream of the dra gene an open reading frame of 313 amino acids was identified. Inactivation of this gene led to an approximately 10-fold increase in the levels of deoxyriboaldolase and pyrimidine nucleoside phosphorylase, and no further induction was seen upon the addition of deoxyribonucleosides. The upstream gene most likely encodes the regulator for the dra-nupC-pdp operon and was designated deoR (stands for deoxyribonucleoside regulator).

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References

Kloudova A, Fucik V . Transport of nucleosides in Bacillus subtilis: characteristics of cytidine-uptake. Nucleic Acids Res. 1974; 1(4):629-37. PMC: 343361. DOI: 10.1093/nar/1.4.629. View

Fucik V, Kloudova A, Holy A . Transport of nucleosides in Bacillus subtilis: the effect of purine nucleosides on the cytidine-uptake. Nucleic Acids Res. 1974; 1(4):639-44. PMC: 343362. DOI: 10.1093/nar/1.4.639. View

MUNCH-PETERSEN A, Schwartz M, Nygaard P . Induction of enzymes involed in the catabolism of deoxyribonucleosides and ribonucleosides in Escherichia coli K 12. Eur J Biochem. 1971; 19(4):533-8. DOI: 10.1111/j.1432-1033.1971.tb01345.x. View

BOYLAN R, Mendelson N, Brooks D, Young F . Regulation of the bacterial cell wall: analysis of a mutant of Bacillus subtilis defective in biosynthesis of teichoic acid. J Bacteriol. 1972; 110(1):281-90. PMC: 247409. DOI: 10.1128/jb.110.1.281-290.1972. View

MUNCH-PETERSEN A, Nygaard P, Fiil N . Mutants constitutive for nucleoside-catabolizing enzymes in Escherichia coli K12. Isolation, charactrization and mapping. Eur J Biochem. 1972; 27(2):208-15. DOI: 10.1111/j.1432-1033.1972.tb01828.x. View

SANGER F, Nicklen S, Coulson A . DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977; 74(12):5463-7. PMC: 431765. DOI: 10.1073/pnas.74.12.5463. View

Valentin-Hansen P, Svenningsen B, MUNCH-PETERSEN A . Regulation of the deo operon in Escherichia coli: the double negative control of the deo operon by the cytR and deoR repressors in a DNA directed in vitro system. Mol Gen Genet. 1978; 159(2):191-202. DOI: 10.1007/BF00270893. View

Birnboim H, DOLY J . A rapid alkaline extraction procedure for screening recombinant plasmid DNA. Nucleic Acids Res. 1979; 7(6):1513-23. PMC: 342324. DOI: 10.1093/nar/7.6.1513. View

Rumiantseva E, Sukhodolets V, Smirnov I . [Production and study of Bacillus subtilis mutants for genes involved in nucleoside catabolism]. Genetika. 1979; 15(3):594-604. View

10.

Hanahan D . Studies on transformation of Escherichia coli with plasmids. J Mol Biol. 1983; 166(4):557-80. DOI: 10.1016/s0022-2836(83)80284-8. View

11.

Maznitsa I, Sukhodolets V, Ukhabotina L . [Cloning of Bacillus subtilis 168 genes compensating for the defect in mutations for thymidine phosphorylase and uridine phosphorylase in Escherichia coli cells]. Genetika. 1983; 19(6):881-7. View

12.

Beaman T, Hitchins A, Ochi K, Vasantha N, Endo T, Freese E . Specificity and control of uptake of purines and other compounds in Bacillus subtilis. J Bacteriol. 1983; 156(3):1107-17. PMC: 217955. DOI: 10.1128/jb.156.3.1107-1117.1983. View

13.

Youngman P, Perkins J, Losick R . A novel method for the rapid cloning in Escherichia coli of Bacillus subtilis chromosomal DNA adjacent to Tn917 insertions. Mol Gen Genet. 1984; 195(3):424-33. DOI: 10.1007/BF00341443. View

14.

Valentin-Hansen P, Hojrup P, Short S . The primary structure of the DeoR repressor from Escherichia coli K-12. Nucleic Acids Res. 1985; 13(16):5927-36. PMC: 321923. DOI: 10.1093/nar/13.16.5927. View

15.

Dandanell G, Valentin-Hansen P, Larsen J, Hammer K . Long-range cooperativity between gene regulatory sequences in a prokaryote. Nature. 1987; 325(6107):823-6. DOI: 10.1038/325823a0. View

16.

Saxild H, Nygaard P . Genetic and physiological characterization of Bacillus subtilis mutants resistant to purine analogs. J Bacteriol. 1987; 169(7):2977-83. PMC: 212336. DOI: 10.1128/jb.169.7.2977-2983.1987. View

17.

Mortensen L, Dandanell G, Hammer K . Purification and characterization of the deoR repressor of Escherichia coli. EMBO J. 1989; 8(1):325-31. PMC: 400807. DOI: 10.1002/j.1460-2075.1989.tb03380.x. View

18.

Walter M, Cook W, Cole L, Short S, Koszalka G, KRENITSKY T . Three-dimensional structure of thymidine phosphorylase from Escherichia coli at 2.8 A resolution. J Biol Chem. 1990; 265(23):14016-22. DOI: 10.2210/pdb1tpt/pdb. View

19.

Sogaard-Andersen L, Martinussen J, Mollegaard N, Douthwaite S, Valentin-Hansen P . The CytR repressor antagonizes cyclic AMP-cyclic AMP receptor protein activation of the deoCp2 promoter of Escherichia coli K-12. J Bacteriol. 1990; 172(10):5706-13. PMC: 526886. DOI: 10.1128/jb.172.10.5706-5713.1990. View

20.

Craig J, Zhang Y, Gallagher M . Cloning of the nupC gene of Escherichia coli encoding a nucleoside transport system, and identification of an adjacent insertion element, IS 186. Mol Microbiol. 1994; 11(6):1159-68. DOI: 10.1111/j.1365-2958.1994.tb00392.x. View