Skip to main content
Log in

An orphangyrB in theMycobacterium smegmatis genome uncovered by comparative genomics

  • Published:
Journal of Genetics Aims and scope Submit manuscript

Abstract

DNA gyrase is an essential topoisomerase found in all bacteria. It is encoded bygyrB andgyrA genes. These genes are organized differently in different bacteria. Direct comparison ofMycobacterium tuberculosis andMycobacterium smegmatis genomes reveals presence of an additionalgyrB inM. smegmatis flanked by novel genes. Analysis of the amino acid sequence of GyrB from different organisms suggests that the orphan GyrB inM. smegmatis may have an important cellular role.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Bachmann B. J. and Low K. B. 1980 Linkage map ofEscherichia coli K-12.Microbiol. Rev. 44, 1–56.

    PubMed  CAS  Google Scholar 

  • Berger J. M., Fass D., Wang J. C. and Harrison S. C. 1998 Structural similarities between topoisomerases that cleave one or both DNA strands.Proc. Natl. Acad. Sci. USA 95, 7876–7881.

    Article  PubMed  CAS  Google Scholar 

  • Brosch R., Gordon S. V., Buchrieser C., Pym A. S., Garnier T. and Cole S. T. 2000 Comparative genomics uncovers large tandem chromosomal duplications inMycobacterium bovis BCG Pasteur.Yeast 17, 111–123.

    Article  PubMed  CAS  Google Scholar 

  • Brown P. O. and Cozzarelli N. R. 1979 A sign inversion mechanism for enzymatic supercoiling of DNA.Science 206, 1081–1083.

    Article  PubMed  CAS  Google Scholar 

  • Champoux J. J. 2001 DNA topoisomerases: structure, function, and mechanism.Annu. Rev. Biochem. 70, 369–413.

    Article  PubMed  CAS  Google Scholar 

  • Chatterji M. and Nagaraja V. 2002 GyrI: a counter-defensive strategy against proteinaceous inhibitors of DNA gyrase.EMBO Reports 3, 261–267.

    Article  PubMed  CAS  Google Scholar 

  • Chatterji M., Unniraman S., Maxwell A. and Nagaraja V. 2000 The additional 165 amino acids in the B protein ofEscherichia coli DNA gyrase have an important role in DNA binding.J. Biol. Chem. 275, 22888–22894.

    Article  PubMed  CAS  Google Scholar 

  • Chatterji M., Unniraman S., Mahadevan S. and Nagaraja V. 2001 Effect of different classes of inhibitors on DNA gyrase fromMycobacterium smegmatis.J. Antimicrob. Chemother. 48, 479–485.

    Article  PubMed  CAS  Google Scholar 

  • Cole S. T., Brosch R., Parkhill J., Garnier T., Churcher C., Harris D.et al. 1998 Deciphering the biology ofMycobacterium tuberculosis from the complete genome sequence.Nature 393, 537–544.

    Article  PubMed  CAS  Google Scholar 

  • Couturier M., Bahassi el-M. and Van Melderen L. 1998 Bacterial death by gyrase poisoning.Trends Microbiol. 6, 269–275.

    Article  PubMed  CAS  Google Scholar 

  • Cozzarelli N. R. 1980 DNA topoisomerases.Cell 22, 327–328.

    Article  PubMed  CAS  Google Scholar 

  • Critchlow S. E., O’Dea M. H., Howells A. J., Couturier M., Gellert M. and Maxwell A. 1997 The interaction of the F plasmid killer protein, CcdB, with DNA gyrase: induction of DNA cleavage and blocking of transcription.J. Mol. Biol. 273, 826–839.

    Article  PubMed  CAS  Google Scholar 

  • Gellert M. 1981 DNA topoisomerases.Annu. Rev. Biochem. 50, 879–910.

    Article  PubMed  CAS  Google Scholar 

  • Gellert M., Mizuuchi K., O’Dea M. H. and Nash H. A. 1976a DNA gyrase: an enzyme that introduces superhelical turns into DNA.Proc. Natl. Acad. Sci. USA 73, 3872–3876.

    Article  PubMed  CAS  Google Scholar 

  • Gellert M., O’Dea M. H., Itoh T. and Tomizawa J. 1976b Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase.Proc. Natl. Acad. Sci. USA 73, 4474–4478.

    Article  PubMed  CAS  Google Scholar 

  • Gellert M., Mizuuchi K., O’Dea M. H., Itoh T. and Tomizawa J. I. 1977 Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity.Proc. Natl. Acad. Sci. USA 74, 4772–4776.

    Article  PubMed  CAS  Google Scholar 

  • Higgins N. P., Peebles C. L., Sugino A. and Cozzarelli N. R. 1978 Purification of subunits ofEscherichia coli DNA gyrase and reconstitution of enzymatic activity.Proc. Natl. Acad. Sci. USA 75, 1773–1777.

    Article  PubMed  CAS  Google Scholar 

  • Klevan L. and Wang J. C. 1980 Deoxyribonucleic acid gyrase-deoxyribonucleic acid complex containing 140 base pairs of deoxyribonucleic acid and an alpha 2 beta 2 protein core.Biochemistry 19, 5229–5234.

    Article  PubMed  CAS  Google Scholar 

  • Liu L. F., Liu C. C. and Alberts B. M. 1980 Type II DNA topo-isomerases: enzymes that can unknot a topologically knotted DNA molecule via a reversible double-strand break.Cell 19, 697–707.

    Article  PubMed  CAS  Google Scholar 

  • Madhusudan K. and Nagaraja V. 1995Mycobacterium smeg-matis DNA gyrase: cloning and overexpression inEscheri-chia coli.Microbiology 141, 3029–3037.

    Article  PubMed  CAS  Google Scholar 

  • Madhusudan K. and Nagaraja V. 1996 Alignment and phyloge-netic analysis of type II DNA topoisomerases.J. Biosci. 21, 613–629.

    Article  CAS  Google Scholar 

  • Madhusudan K., Ramesh V. and Nagaraja V. 1994 Molecular cloning ofgyrA andgyrB genes ofMycobacterium tuberculosis: analysis of nucleotide sequence.Biochem. Mol. Biol. Int. 33, 651–660.

    PubMed  CAS  Google Scholar 

  • Manjunatha U. H., Madhusudan K., Visweswariah S. S. and Nagaraja V. 2000 Structural heterogeneity in DNA gyrase in Gram-positive and Gram-negative bacteria.Curr. Sci. 78, 968–974.

    Google Scholar 

  • Manjunatha U. H., Mahadevan S., Visweswariah S. S. and Nagaraja V. 2001a Monoclonal antibodies to mycobacterial DNA gyrase A inhibit DNA supercoiling activity.Eur. J. Biochem. 268, 2038–2046.

    Article  PubMed  CAS  Google Scholar 

  • Manjunatha U. H., Somesh B. P., Nagaraja V. and Visweswariah S. S. 2001b AMycobacterium smegmatis gyrase B specific monoclonal antibody reveals association of gyrase A and B subunits in the cell.FEMS Microbiol. Lett. 194, 87–92.

    Article  PubMed  CAS  Google Scholar 

  • Manjunatha U. H., Dalal M., Chatterji M., Radha D. R., Visweswariah S. S. and Nagaraja V. 2002 Functional characterisation of mycobacterial DNA gyrase: an efficient decatenase.Nucl. Acids Res. 30, 2144–2153.

    Article  PubMed  CAS  Google Scholar 

  • Maxwell A. 1997 DNA gyrase as a drug target.Trends Microbiol. 5, 102–109.

    Article  PubMed  CAS  Google Scholar 

  • Maxwell A. and Gellert M. 1986 Mechanistic aspects of DNA topoisomerases.Adv. Protein Chem. 38, 69–107.

    Article  PubMed  CAS  Google Scholar 

  • Neumann S., Simon H., Zimmer C. and Quinones A. 1996 The antitumor agent cisplatin inhibits DNA gyrase and preferentially inducesgyrB gene expression inEscherichia coli.Biol. Chem. 377, 731–739.

    PubMed  CAS  Google Scholar 

  • Reece R. J. and Maxwell A. 1991 DNA gyrase: structure and function.Crit. Rev. Biochem. Mol. Biol. 26, 335–375.

    PubMed  CAS  Google Scholar 

  • Salazar L., Fsihi H., de Rossi E., Riccardi G., Rios C., Cole S. T. and Takiff H. E. 1996 Organisation of the origins of replication of the chromosomes ofMycobacterium smegmatis, Mycobacterium leprae andMycobacterium tuberculosis and isolation of a functional origin fromM. smegmatis.Mol. Microbiol. 20, 283–293.

    Article  PubMed  CAS  Google Scholar 

  • Sugino A., Peebles C. L., Kreuzer K. N. and Cozzarelli N. R. 1977 Mechanism of action of nalidixic acid: purification ofEscherichia coli nalA gene product and its relationship to DNA gyrase and a novel nicking-closing enzyme.Proc. Natl. Acad. Sci. USA 74, 4767–4771.

    Article  PubMed  CAS  Google Scholar 

  • Sugino A., Higgins N. P. and Cozzarelli N. R. 1980 DNA gyrase subunit stoichiometry and the covalent attachment of subunit A to DNA during DNA cleavage.Nucl. Acids Res. 8, 3865–3874.

    Article  PubMed  CAS  Google Scholar 

  • Thiara A. S. and Cundliffe E. 1993 Expression and analysis of twogyrB genes from the novobiocin producer,Streptomyces sphaeroides.Mol. Microbiol. 8, 495–506.

    Article  PubMed  CAS  Google Scholar 

  • Unniraman S. and Nagaraja V. 1999 Regulation of DNA gyrase operon inMycobacterium smegmatis: a distinct mechanism of relaxation stimulated transcription.Genes Cells 4, 697–706.

    Article  PubMed  CAS  Google Scholar 

  • Unniraman S., Chatterji M. and Nagaraja V. 2002 DNA gyrase genes inMycobacterium tuberculosis: a single operon driven by multiple promoters.J. Bacteriol. 184, 5449–5456.

    Article  PubMed  CAS  Google Scholar 

  • Vizan J. L., Hernandez-Chico C., del Castillo I. and Moreno F. 1991 The peptide antibiotic microcin B17 induces double-strand cleavage of DNA mediated byE. coli DNA gyrase.EMBO J. 10, 467–476.

    PubMed  CAS  Google Scholar 

  • Wang J. C. 1996 DNA topoisomerases.Annu. Rev. Biochem. 65, 635–692.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to V. Nagaraja.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jain, P., Nagaraja, V. An orphangyrB in theMycobacterium smegmatis genome uncovered by comparative genomics. J Genet 81, 105–110 (2002). https://doi.org/10.1007/BF02715907

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02715907

Keywords

Navigation