Skip to main content
PMC home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1984 Jul;81(13):4046–4050. doi: 10.1073/pnas.81.13.4046

Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature.

E Goldstein, K Drlica
PMCID: PMC345365  PMID: 6377307

Abstract

The level of DNA supercoiling can be altered either by breaking-rejoining reactions that change the DNA linking number or by environmental changes that alter the helical pitch of DNA. In vitro, temperature changes alter helical pitch and, thus, supercoiling. We find that plasmids isolated from bacteria grown at different temperatures exhibit differences in DNA linking numbers. The differences in plasmid linking numbers offset the effect temperature is expected to have on supercoiling. These results are consistent with the hypothesis that fine control of DNA topology in bacterial cells is brought about by changes in linking number to maintain a constant value for supercoiling.

Full text

PDF
4048

Images in this article

4047Image
on p.4047
4048Image
on p.4048
4048Image
on p.4048
4048Image
on p.4048

Selected References

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

  1. Anderson P., Bauer W. Supercoiling in closed circular DNA: dependence upon ion type and concentration. Biochemistry. 1978 Feb 21;17(4):594–601. doi: 10.1021/bi00597a006. [DOI] [PubMed] [Google Scholar]
  2. Bolivar F., Rodriguez R. L., Betlach M. C., Boyer H. W. Construction and characterization of new cloning vehicles. I. Ampicillin-resistant derivatives of the plasmid pMB9. Gene. 1977;2(2):75–93. doi: 10.1016/0378-1119(77)90074-9. [DOI] [PubMed] [Google Scholar]
  3. Cozzarelli N. R. DNA gyrase and the supercoiling of DNA. Science. 1980 Feb 29;207(4434):953–960. doi: 10.1126/science.6243420. [DOI] [PubMed] [Google Scholar]
  4. Deniss I. S., Morgan A. R. Studies on the mechanism of DNA cleavage by ethidium. Nucleic Acids Res. 1976 Feb;3(2):315–323. doi: 10.1093/nar/3.2.315. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Depew D. E., Wang J. C. Conformational fluctuations of DNA helix. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4275–4279. doi: 10.1073/pnas.72.11.4275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. DiNardo S., Voelkel K. A., Sternglanz R., Reynolds A. E., Wright A. Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell. 1982 Nov;31(1):43–51. doi: 10.1016/0092-8674(82)90403-2. [DOI] [PubMed] [Google Scholar]
  7. Drlica K., Snyder M. Superhelical Escherichia coli DNA: relaxation by coumermycin. J Mol Biol. 1978 Apr 5;120(2):145–154. doi: 10.1016/0022-2836(78)90061-x. [DOI] [PubMed] [Google Scholar]
  8. Filutowicz M., Jonczyk P. Essential role of the gyrB gene product in the transcriptional event coupled to dnaA-dependent initiation of Escherichia coli chromosome replication. Mol Gen Genet. 1981;183(1):134–138. doi: 10.1007/BF00270151. [DOI] [PubMed] [Google Scholar]
  9. Gellert M. DNA topoisomerases. Annu Rev Biochem. 1981;50:879–910. doi: 10.1146/annurev.bi.50.070181.004311. [DOI] [PubMed] [Google Scholar]
  10. Gellert M., Mizuuchi K., O'Dea M. H., Itoh T., Tomizawa J. I. Nalidixic acid resistance: a second genetic character involved in DNA gyrase activity. Proc Natl Acad Sci U S A. 1977 Nov;74(11):4772–4776. doi: 10.1073/pnas.74.11.4772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Gellert M., O'Dea M. H., Itoh T., Tomizawa J. Novobiocin and coumermycin inhibit DNA supercoiling catalyzed by DNA gyrase. Proc Natl Acad Sci U S A. 1976 Dec;73(12):4474–4478. doi: 10.1073/pnas.73.12.4474. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Herendeen S. L., VanBogelen R. A., Neidhardt F. C. Levels of major proteins of Escherichia coli during growth at different temperatures. J Bacteriol. 1979 Jul;139(1):185–194. doi: 10.1128/jb.139.1.185-194.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Holmes D. S., Quigley M. A rapid boiling method for the preparation of bacterial plasmids. Anal Biochem. 1981 Jun;114(1):193–197. doi: 10.1016/0003-2697(81)90473-5. [DOI] [PubMed] [Google Scholar]
  14. Isberg R. R., Syvanen M. DNA gyrase is a host factor required for transposition of Tn5. Cell. 1982 Aug;30(1):9–18. doi: 10.1016/0092-8674(82)90006-x. [DOI] [PubMed] [Google Scholar]
  15. Kano Y., Miyashita T., Nakamura H., Kuroki K., Nagata A., Imamoto F. In vivo correlation between DNA supercoiling and transcription. Gene. 1981 Mar;13(2):173–184. doi: 10.1016/0378-1119(81)90006-8. [DOI] [PubMed] [Google Scholar]
  16. Kreuzer K. N., Cozzarelli N. R. Escherichia coli mutants thermosensitive for deoxyribonucleic acid gyrase subunit A: effects on deoxyribonucleic acid replication, transcription, and bacteriophage growth. J Bacteriol. 1979 Nov;140(2):424–435. doi: 10.1128/jb.140.2.424-435.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lemaux P. G., Herendeen S. L., Bloch P. L., Neidhardt F. C. Transient rates of synthesis of individual polypeptides in E. coli following temperature shifts. Cell. 1978 Mar;13(3):427–434. doi: 10.1016/0092-8674(78)90317-3. [DOI] [PubMed] [Google Scholar]
  18. Lockshon D., Morris D. R. Positively supercoiled plasmid DNA is produced by treatment of Escherichia coli with DNA gyrase inhibitors. Nucleic Acids Res. 1983 May 25;11(10):2999–3017. doi: 10.1093/nar/11.10.2999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Lusk J. E., Williams R. J., Kennedy E. P. Magnesium and the growth of Escherichia coli. J Biol Chem. 1968 May 25;243(10):2618–2624. [PubMed] [Google Scholar]
  20. Manes S. H., Pruss G. J., Drlica K. Inhibition of RNA synthesis by oxolinic acid is unrelated to average DNA supercoiling. J Bacteriol. 1983 Jul;155(1):420–423. doi: 10.1128/jb.155.1.420-423.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Menzel R., Gellert M. Regulation of the genes for E. coli DNA gyrase: homeostatic control of DNA supercoiling. Cell. 1983 Aug;34(1):105–113. doi: 10.1016/0092-8674(83)90140-x. [DOI] [PubMed] [Google Scholar]
  22. Mukai F. H., Margolin P. ANALYSIS OF UNLINKED SUPPRESSORS OF AN O degrees MUTATION IN SALMONELLA. Proc Natl Acad Sci U S A. 1963 Jul;50(1):140–148. doi: 10.1073/pnas.50.1.140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Neidhardt F. C., VanBogelen R. A. Positive regulatory gene for temperature-controlled proteins in Escherichia coli. Biochem Biophys Res Commun. 1981 May 29;100(2):894–900. doi: 10.1016/s0006-291x(81)80257-4. [DOI] [PubMed] [Google Scholar]
  24. Orr E., Fairweather N. F., Holland I. B., Pritchard R. H. Isolation and characterisation of a strain carrying a conditional lethal mutation in the cou gene of Escherichia coli K12. Mol Gen Genet. 1979;177(1):103–112. doi: 10.1007/BF00267259. [DOI] [PubMed] [Google Scholar]
  25. Pettijohn D. E., Pfenninger O. Supercoils in prokaryotic DNA restrained in vivo. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1331–1335. doi: 10.1073/pnas.77.3.1331. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pruss G. J., Manes S. H., Drlica K. Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell. 1982 Nov;31(1):35–42. doi: 10.1016/0092-8674(82)90402-0. [DOI] [PubMed] [Google Scholar]
  27. Pulleyblank D. E., Shure M., Tang D., Vinograd J., Vosberg H. P. Action of nicking-closing enzyme on supercoiled and nonsupercoiled closed circular DNA: formation of a Boltzmann distribution of topological isomers. Proc Natl Acad Sci U S A. 1975 Nov;72(11):4280–4284. doi: 10.1073/pnas.72.11.4280. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Ryals J., Little R., Bremer H. Temperature dependence of RNA synthesis parameters in Escherichia coli. J Bacteriol. 1982 Aug;151(2):879–887. doi: 10.1128/jb.151.2.879-887.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. SCHAECHTER M., MAALOE O., KJELDGAARD N. O. Dependency on medium and temperature of cell size and chemical composition during balanced grown of Salmonella typhimurium. J Gen Microbiol. 1958 Dec;19(3):592–606. doi: 10.1099/00221287-19-3-592. [DOI] [PubMed] [Google Scholar]
  30. Shure M., Pulleyblank D. E., Vinograd J. The problems of eukaryotic and prokaryotic DNA packaging and in vivo conformation posed by superhelix density heterogeneity. Nucleic Acids Res. 1977;4(5):1183–1205. doi: 10.1093/nar/4.5.1183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Sinden R. R., Carlson J. O., Pettijohn D. E. Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: analogous measurements in insect and human cells. Cell. 1980 Oct;21(3):773–783. doi: 10.1016/0092-8674(80)90440-7. [DOI] [PubMed] [Google Scholar]
  32. Sinden R. R., Pettijohn D. E. Torsional tension in intracellular bacteriophage T4 DNA. Evidence that a linear DNA duplex can be supercoiled in vivo. J Mol Biol. 1982 Dec 15;162(3):659–677. doi: 10.1016/0022-2836(82)90394-1. [DOI] [PubMed] [Google Scholar]
  33. Smith G. R. DNA supercoiling: another level for regulating gene expression. Cell. 1981 Jun;24(3):599–600. doi: 10.1016/0092-8674(81)90085-4. [DOI] [PubMed] [Google Scholar]
  34. Steck T. R., Pruss G. J., Manes S. H., Burg L., Drlica K. DNA supercoiling in gyrase mutants. J Bacteriol. 1984 May;158(2):397–403. doi: 10.1128/jb.158.2.397-403.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Sternglanz R., DiNardo S., Voelkel K. A., Nishimura Y., Hirota Y., Becherer K., Zumstein L., Wang J. C. Mutations in the gene coding for Escherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci U S A. 1981 May;78(5):2747–2751. doi: 10.1073/pnas.78.5.2747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Sutcliffe J. G. Complete nucleotide sequence of the Escherichia coli plasmid pBR322. Cold Spring Harb Symp Quant Biol. 1979;43(Pt 1):77–90. doi: 10.1101/sqb.1979.043.01.013. [DOI] [PubMed] [Google Scholar]
  37. Trucksis M., Golub E. I., Zabel D. J., Depew R. E. Escherichia coli and Salmonella typhimurium supX genes specify deoxyribonucleic acid topoisomerase I. J Bacteriol. 1981 Aug;147(2):679–681. doi: 10.1128/jb.147.2.679-681.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Vinograd J., Lebowitz J., Radloff R., Watson R., Laipis P. The twisted circular form of polyoma viral DNA. Proc Natl Acad Sci U S A. 1965 May;53(5):1104–1111. doi: 10.1073/pnas.53.5.1104. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Wang J. C. Degree of superhelicity of covalently closed cyclic DNA's from Escherichia coli. J Mol Biol. 1969 Jul 28;43(2):263–272. doi: 10.1016/0022-2836(69)90266-6. [DOI] [PubMed] [Google Scholar]
  40. Wang J. C., Peck L. J., Becherer K. DNA supercoiling and its effects on DNA structure and function. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 1):85–91. doi: 10.1101/sqb.1983.047.01.011. [DOI] [PubMed] [Google Scholar]
  41. Yamamori T., Yura T. Temperature-induced synthesis of specific proteins in Escherichia coli: evidence for transcriptional control. J Bacteriol. 1980 Jun;142(3):843–851. doi: 10.1128/jb.142.3.843-851.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. von Wright A., Bridges B. A. Effect of gyrB-mediated changes in chromosome structure on killing of Escherichia coli by ultraviolet light: experiments with strains differing in deoxyribonucleic acid repair capacity. J Bacteriol. 1981 Apr;146(1):18–23. doi: 10.1128/jb.146.1.18-23.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES