Changes in the linking number of supercoiled DNA accompany growth transitions in Escherichia coli

The supercoiling levels of plasmid DNA were determined from Escherichia coli which was grown in ways that are known to alter global patterns of gene expression and metabolism. Changes in DNA supercoiling were shown to occur during several types of these nutrient upshifts and downshifts. The most dramatic change in supercoiling was seen in starved cells, in which two populations of differentially relaxed plasmids were shown to coexist. Thus, some changes in the external nutritional environment that cause the cells to reorganize their global metabolism also cause accompanying changes in DNA supercoiling. Results of experiments with dinitrophenol suggested that the observed relaxations were probably not due to reduced pools of ATP. When rifampin was used to release supercoils restrained by RNA polymerase, the cellular topoisomerases responded by removing these new, unrestrained supercoils. We interpret these results as implying that the cellular topological machinery maintains a constant superhelical energy in the DNA except during certain growth transitions, when changes in metabolism and gene expression are accompanied by changes in DNA supercoiling.

[1]  M. Gellert,et al.  DNA gyrase: an enzyme that introduces superhelical turns into DNA. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[2]  G. Pruss DNA topoisomerase I mutants. Increased heterogeneity in linking number and other replicon-dependent changes in DNA supercoiling. , 1985, Journal of molecular biology.

[3]  H. Vosberg DNA topoisomerases: enzymes that control DNA conformation. , 1985, Current topics in microbiology and immunology.

[4]  J. Wong,et al.  Regulation of ribonucleic acid accumulation in vivo by nucleoside triphosphates. , 1972, The Journal of biological chemistry.

[5]  I. Pastan,et al.  Cyclic AMP regulates Catabolite and Transient Repression in E. coli , 1969, Nature.

[6]  E. Wahle,et al.  Gene expression in a temperature‐sensitive gyrB mutant of Escherichia coli. , 1984, The EMBO journal.

[7]  Y. Tse‐Dinh Regulation of the Escherichia coli DNA topoisomerase I gene by DNA supercoiling , 1985, Nucleic Acids Res..

[8]  B. Oostra,et al.  Enhancement of ribosomal ribonucleic acid synthesis by deoxyribonucleic acid gyrase activity in Escherichia coli , 1981, Journal of bacteriology.

[9]  W. Keller Determination of the number of superhelical turns in simian virus 40 DNA by gel electrophoresis. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[10]  K. Drlica,et al.  Biology of bacterial deoxyribonucleic acid topoisomerases. , 1984, Microbiological reviews.

[11]  C. Smith,et al.  Promoter-specific inhibition of transcription by antibiotics which act on DNA gyrase , 1978, Nature.

[12]  N. Yamamoto,et al.  Mechanisms determining aerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[13]  O. H. Lowry,et al.  The effect of carbon and nitrogen sources on the level of metabolic intermediates in Escherichia coli. , 1971, The Journal of biological chemistry.

[14]  D. Nierlich Regulation of bacterial growth, RNA, and protein synthesis. , 1978, Annual review of microbiology.

[15]  S. Gottesman Bacterial regulation: global regulatory networks. , 1984, Annual review of genetics.

[16]  Howard B. Gamper,et al.  A topological model for transcription based on unwinding angle analysis of E. coli RNA polymerase binary, initiation and ternary complexes , 1982, Cell.

[17]  V. Vagner,et al.  Activation and inhibition of transcription by supercoiling. , 1985, Journal of molecular biology.

[18]  B. Sanzey,et al.  Modulation of gene expression by drugs affecting deoxyribonucleic acid gyrase , 1979, Journal of bacteriology.

[19]  D. Lockshon,et al.  Positively supercoiled plasmid DNA is produced by treatment of Escherichia coli with DNA gyrase inhibitors. , 1983, Nucleic acids research.

[20]  L. Freedman,et al.  Genetic dissection of stringent control and nutritional shift-up response of the Escherichia coli S10 ribosomal protein operon. , 1985, Journal of molecular biology.

[21]  D. Lilley,et al.  The genetic control of DNA supercoiling in Salmonella typhimurium. , 1984, The EMBO journal.

[22]  K. Drlica,et al.  Regulation of bacterial DNA supercoiling: plasmid linking numbers vary with growth temperature. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[23]  M. Gellert,et al.  Regulation of the genes for E. coli DNA gyrase: Homeostatic control of DNA supercoiling , 1983, Cell.

[24]  R. Sternglanz,et al.  Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes , 1982, Cell.

[25]  H. Shuman,et al.  The effect of nalidixic acid on the expression of some genes in Escherichia coli K-12. , 1975, Biochemical and biophysical research communications.

[26]  R. Sinden,et al.  Torsional tension in the DNA double helix measured with trimethylpsoralen in living E. coli cells: Analogous measurements in insect and human cells , 1980, Cell.

[27]  M. Hoagland,et al.  Polyribosomes of Escherichia coli. Breakdown during glucose starvation. , 1967, The Journal of biological chemistry.

[28]  F. Neidhardt,et al.  Culture Medium for Enterobacteria , 1974, Journal of bacteriology.

[29]  J. Gralla,et al.  All three elements of the lac ps promoter mediate its transcriptional response to DNA supercoiling. , 1987, Journal of molecular biology.

[30]  K. Drlica,et al.  Topoisomerase I mutants: the gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[31]  L. Lindahl,et al.  Transcription of ribosomal genes during a nutritional shift-up of Escherichia coli , 1986, Journal of bacteriology.

[32]  K. Drlica,et al.  Escherichia coli DNA topoisomerase I mutants: Increased supercoiling is corrected by mutations near gyrase genes , 1982, Cell.

[33]  J. Gralla,et al.  Supercoiling response of the lac ps promoter in vitro. , 1985, Journal of molecular biology.

[34]  J. Vinograd,et al.  The problems of eukaryotic and prokaryotic DNA packaging and in vivo conformation posed by superhelix density heterogeneity. , 1977, Nucleic acids research.

[35]  D. Holmes,et al.  A rapid boiling method for the preparation of bacterial plasmids. , 1981, Analytical biochemistry.

[36]  N. Cozzarelli,et al.  Escherichia coli type-1 topoisomerases: identification, mechanism, and role in recombination. , 1983, Cold Spring Harbor symposia on quantitative biology.

[37]  A. Hershko,et al.  Influence of protease inhibitors and energy metabolism on intracellular protein breakdown in starving Escherichia coli. , 1973, Biochemical and biophysical research communications.

[38]  W. Donachie,et al.  Growth of the Bacterial Cell , 1970, Nature.

[39]  A. L. Koch,et al.  Protein degradation in Escherichia coli. II. Strain differences in the degradation of protein and nucleic acid resulting from starvation. , 1971, The Journal of biological chemistry.