The Genetic Control of DNA Supercoiling in Salmonella Typhimurium

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1984 Aug 1

PMID 6090123

Citations 52

Authors

S M Richardson

C F Higgins

D M Lilley

Affiliations

Soon will be listed here.

Abstract

We have elucidated the genetic control of DNA supercoiling in Salmonella typhimurium. The level of superhelix density is controlled by two classes of genes. The only member of the first class is topA, the structural gene for topoisomerase I. The second class, tos, (topoisomerase one suppressor) consists of at least two genes, one of which is linked to gyrA, the structural gene for the topoisomerase subunit of DNA gyrase. Deletions of topA result in oversupercoiling of plasmid DNA. These mutations do not require the acquisition of second-site compensatory mutations to allow cell growth, in contrast to the situation in Escherichia coli. However, tos mutations, unlinked to topA, have been isolated which reduce plasmid superhelix density. We conclude that the level of DNA supercoiling in S. typhimurium is a dynamic balance between the effects of the gene products of topA (relaxation) and tos (supercoiling) which act independently of each other. Using a variety of combinations of these mutations we have constructed a series of isogenic strains, each of which has a different but precisely defined level of plasmid supercoiling; the series as a whole provides a wide range of supercoiling both above and below the wild-type level.

Citing Articles

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Topoisomerase I Essentiality, DnaA-Independent Chromosomal Replication, and Transcription-Replication Conflict in Escherichia coli.

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Yan R, Hu S, Ma N, Song P, Liang Q, Zhang H Int J Mol Sci. 2019; 20(5).

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References

Isberg R, Syvanen M . DNA gyrase is a host factor required for transposition of Tn5. Cell. 1982; 30(1):9-18. DOI: 10.1016/0092-8674(82)90006-x. View

Sanderson K, Roth J . Linkage map of Salmonella typhimurium, Edition VI. Microbiol Rev. 1983; 47(3):410-53. PMC: 281582. DOI: 10.1128/mr.47.3.410-453.1983. View

Clewell D, Helinski D . Supercoiled circular DNA-protein complex in Escherichia coli: purification and induced conversion to an opern circular DNA form. Proc Natl Acad Sci U S A. 1969; 62(4):1159-66. PMC: 223628. DOI: 10.1073/pnas.62.4.1159. View

Sternglanz R, DiNardo S, Voelkel K, Nishimura Y, Hirota Y, Becherer K . Mutations in the gene coding for Escherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci U S A. 1981; 78(5):2747-51. PMC: 319434. DOI: 10.1073/pnas.78.5.2747. View

DUBNAU E, Margolin P . Suppression of promoter mutations by the pleiotropic supx mutations. Mol Gen Genet. 1972; 117(2):91-112. DOI: 10.1007/BF00267607. View

Smith C, Kubo M, Imamoto F . Promoter-specific inhibition of transcription by antibiotics which act on DNA gyrase. Nature. 1978; 275(5679):420-3. DOI: 10.1038/275420a0. View

SCHMIEGER H . A method for detection of phage mutants with altered transducing ability. Mol Gen Genet. 1971; 110(4):378-81. DOI: 10.1007/BF00438281. View

Bochner B, Huang H, Schieven G, Ames B . Positive selection for loss of tetracycline resistance. J Bacteriol. 1980; 143(2):926-33. PMC: 294396. DOI: 10.1128/jb.143.2.926-933.1980. View

Pulleyblank D, Shure M, Tang D, Vinograd J, Vosberg H . 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; 72(11):4280-4. PMC: 388704. DOI: 10.1073/pnas.72.11.4280. View

10.

Sanzey B . Modulation of gene expression by drugs affecting deoxyribonucleic acid gyrase. J Bacteriol. 1979; 138(1):40-7. PMC: 218235. DOI: 10.1128/jb.138.1.40-47.1979. View

11.

Chelala C, Margolin P . Effects of deletions on cotransduction linkage in Salmonella typhimurium: evidence that bacterial chromosome deletions affect the formation of transducing DNA fragments. Mol Gen Genet. 1974; 131(2):97-112. DOI: 10.1007/BF00266146. View

12.

Bachmann B . Linkage map of Escherichia coli K-12, edition 7. Microbiol Rev. 1983; 47(2):180-230. PMC: 281571. DOI: 10.1128/mr.47.2.180-230.1983. View

13.

Wang J, Peck L, 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. View

14.

Drlica K, Snyder M . Superhelical Escherichia coli DNA: relaxation by coumermycin. J Mol Biol. 1978; 120(2):145-54. DOI: 10.1016/0022-2836(78)90061-x. View

15.

Trucksis M, Depew R . Identification and localization of a gene that specifies production of Escherichia coli DNA topoisomerase I. Proc Natl Acad Sci U S A. 1981; 78(4):2164-8. PMC: 319304. DOI: 10.1073/pnas.78.4.2164. View

16.

Mukai F, Margolin P . ANALYSIS OF UNLINKED SUPPRESSORS OF AN O degrees MUTATION IN SALMONELLA. Proc Natl Acad Sci U S A. 1963; 50(1):140-8. PMC: 300667. DOI: 10.1073/pnas.50.1.140. View

17.

Mizuuchi K, Gellert M, WEISBERG R, NASH H . Catenation and supercoiling in the products of bacteriophage lambda integrative recombination in vitro. J Mol Biol. 1980; 141(4):485-94. DOI: 10.1016/0022-2836(80)90256-9. View

18.

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

19.

Pruss G, Manes S, Drlica K . Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell. 1982; 31(1):35-42. DOI: 10.1016/0092-8674(82)90402-0. View

20.

Wang J . Interaction between DNA and an Escherichia coli protein omega. J Mol Biol. 1971; 55(3):523-33. DOI: 10.1016/0022-2836(71)90334-2. View