Abstract
This study uncovers a new mechanism of regulation of DNA supercoiling operativein vivo upon an aerobic-anaerobic transition inEscherichia coli. Exponentially growing aerobic batch cultures were subjected to a shift to anaerobic conditions. The ratio [ATP]/[ADP] remained essentially constant at 8.5 in the aerobic culture and after a transition to anaerobiosis while DNA supercoiling increased noticeably upon anaerobiosis. This result indicated that the mechanism of regulation of DNA supercoiling by the [ATP]/[ADP] ratio was not operative. The increase in DNA supercoiling was followed by a large decrease in the DNA-relaxing activity of topoisomerase I while gyrase activity remained relatively constant. This decrease in the activity of topoisomerase I is likely to be responsible for the increase in DNA supercoiling.
Similar content being viewed by others
Abbreviations
- TPE:
-
Tris-phosphate-EDTA buffer
- TBE:
-
Tris-borate-EDTA buffer
References
Neidhardt FC: Multigene systems and regulons. In: FC Neidhardt et al. (eds)Escherichia coli andSalmonella typhimurium Cellular and Molecular Biology, ASM Press, Washington DC, 1987 pp 1313–1318
Clark DP: The fermentation pathways inEscherichia coli. FEMS Microbiol Rev 63:223–234, 1989
Smith MW, Neidhardt FC: Proteins induced by anaerobiosis inEscherichia coli. J Bacteriol 154:336–343, 1983
Ni Bhriain N, Dorman CJ, Higgins CF: An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinate regulation of gene expression. Mol Microbiol 3:933–942, 1989
Pruss GJ, Drlica K: DNA supercoiling and prokaryotic transcription. Cell 56:521–523, 1989
Pruss GJ, Drlica K: Topoisomerase I mutants: The gene on pBR322 that encodes resistance to tetracycline affects plasmid DNA supercoiling. Proc Natl Acad Sci USA 83:8952–8956, 1986
Menzel R, Gellert M: Regulation of the genes forE. coli DNA gyrase: Homeostatic control of DNA supercoiling. Cell 34:105–113, 1983
Gellert M, Mizuuchi K, O'Dea MH, Nash HA: DNA gyrase: An enzyme that introduces superhelical turns into DNA. Proc Natl Acad Sci USA 73:3872–3876 1976
Westerhoff HV, O'Dea MH, Maxwell A, Gellert M: DNA supercoiling by DNA gyrase. A static head analysis. Cell Biophys 12:157–181, 1988
Hsieh LS, Burger RM, Drlica K: Bacterial DNA supercoiling and ATP/ADP changes associated to transition to anaerobic growth. J Mol Biol 199:443–450, 1991
Hsieh LS, Rouviere-Yaniv J, Drlica K: Bacterial DNA supercoiling and ATP/ADP ratio: changes associated with salt shock. J Bacteriol 173:3914–3917, 1991
Sternglanz R, DiNardo S, Voelkel KA, Nishimura Y, Hirota Y, Becherer K, Zumstein L, Wang JC: Mutations in the gene coding forEscherichia coli DNA topoisomerase I affect transcription and transposition. Proc Natl Acad Sci USA 78:2747–2751, 1981
Lamprecht W, Trautschold I: In: HU Bergmeyer (ed) Methods of enzymatic analysis, vol. 4. Verlag Chemie, Weinheim, 1974, pp 2201–2210
Bakker EP, Magerich WE: Interconversion of components of the bacterial proton motive force by electrogenic potassium transport. J Bacteriol 147:820–826, 1981
Kashket ER: Stoichiometry of the H+-ATPase of growing and resting, aerobicEscherichia coli. Biochemistry 21:5534–5538, 1982
Bakker EP: Accumulation of thallous ions (Tl+) as a measure of the electrical potential difference across the cytoplasmic membrane of bacteria. Biochemistry 17:2899–2904, 1978
Wu H, Shyy S, Wang JC, Liu LF: Transcription generates positively and negatively supercoiled domains in the template. Cell 53:433–440, 1988
Gober JW, Kashket ER: Role of DNA superhelicity in regulation of bacteroid-associated functions ofBradyhyzobium sp. strain 32H1. App Environm Microbiol 55:1420–1425, 1989
de Jong S, Zijlstra JG, de Vries EGE, Mulder NH: Reduced DNA topoisomerase II activity and drug-induced DNA cleavage activity in an adriamycin-resistant human small cell lung carcinoma cell line. Cancer Res 50:304–309, 1990
Tempest JW, Neijssel OM: The status ofYATP and maintenance energy as biologically interpretable phenomena. Ann Rev Microbiol 38:459–486, 1984
Verdoni N, Aon MA, Lebeault J-M, Thomas D: Proton motive force, energy recycling by end-product excretion, and metabolic uncoupling during anaerobic growth ofPseudomonas mendocina. J Bacteriol 172:6673–6681, 1990
Yamamoto N, Droffner ML: Mechanisms determining aerobic or anaerobic growth in the facultative anaerobeSalmonella typhimurium. Proc Natl Acad Sci USA 82:2077–2081, 1985
Balke VL, Gralla JD: Changes in the linking number of supercoiled DNA accompany growth transitions inEscherichia coli. J Bacteriol 169:4499–4506, 1987
Drlica K: Bacterial topoisomerases and the control of DNA supercoiling. Trends Genet 6:433–437, 1990
Dietzler DN, Leckie MP, Sternheim WL, Ungar JM Crimmins DL, Lewis JW: Regulation of glycogen synthesis and glucose utilization inEscherichia coli during maintenance of the energy charge. J Biol Chem 254:8276–8287, 1979
Dietzler DN, Leckie MP, Lewis JW, Porter SE, Taxman TL, Lais CJ: Evidence for new factors in the coordinate regulation of energy metabolism inEscherichia coli. J Biol Chem 254:8295–8307, 1979
Westerhoff HV, Van Dam K: Thermodynamics and Control of Biological Free-Energy Transduction. Elsevier, Amsterdam, 1987
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Cortassa, S., Aon, M.A. Altered topoisomerase activities may be involved in the regulation of DNA supercoiling in aerobic-anaerobic transitions inEscherichia coli . Mol Cell Biochem 126, 115–124 (1993). https://doi.org/10.1007/BF00925689
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00925689