Summary
The mechanism of anaerobic regulation of synthesis of colicins E1, E2, E3, K and D was studied. It was found that anaerobiosis significantly increases expression of the genes for colicins E1, E2, E3, K, and D. Experiments with novobiocin (a DNA gyrase inhibitor) showed that colicin synthesis in minicells and derepressed colicin synthesis in cells are dramatically reduced by relaxation of DNA supercoiling. A good correlation was observed between the levels of colicin synthesis and plasmid DNA supercoiling and the degree of aeration of the cultures. Thus, the regulation of colicin gene expression in response to a change in aeration appears to be mediated by environmentally induced variations in DNA supercoiling.
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References
Aliabadi Z, Park YK, Slonzewski JL, Foster JW (1988) Novel regulatory loci controlling oxygen- and pH-regulated gene expression in Salmonella typhimurium. J Bacteriol 170:842–851
Andersen KB, von Meyenburg K (1980) Are growth rates of Escherichia coli in batch cultures limited by respiration? J Bacteriol 144:114–123
Axley MJ, Stadtman TC (1988) Anaerobic induction of Escherichia coli formate dehydrogenase (hydrogenase-linked) is enhanced by gyrase inactivation. Proc Nail Acad Sci USA 85:1023–1027
DiNardo SK, Voelkel KA, Sternglanz R, Reynolds AE, Wright A (1982) Escherichia coli DNA topoisomerase I mutants have compensatory mutations in DNA gyrase genes. Cell 31:43–51
Dorman CJ, Barr GC, Ni Bhriain N, Higgins CF (1988) DNA supercoiling and the anaerobic and growth phase regulation of tonB gene expression. J Bacteriol 170:2816–2826
Drlica K (1984) Biology of bacterial deoxyribonucleic acid topoisomerases. Microbiol Rev 48:273–289
Hardy KG, Harwood CR, Meynell GG (1974) Expression of colicin factor E2-P9. Mol Gen Genet 131:313–331
Higgins CF, Dorman CJ, Stirling DA, Waddell L, Booth JR, May G, Bremer E (1988) A physiological role for DNA supercoiling in the osmotic regulation of gene expression in S. typhimurium and E. coli. Cell 52:569–584
Jamieson DJ, Higgins CF (1986) Two genetically distinct pathways for transcriptional regulation of anaerobic gene expression in Salmonella typhimurium. J Bacteriol 168:389–397
Konisky J (1982) Colicins and other bacteriocins with established modes of action. Annu Rev Microbiol 36:125–144
Kranz RG, Haselkorn R (1986) Anaerobic regulation of nitrogen-fixation genes in Rhodopseudomonas capsulata. Proc Natl Acad Sci USA 83:6805–6809
Laemmli UK (1970) Cleavage of structural proteins during the assembly of head of bacteriophage T4. Nature 227:680–685
Lambden PR, Guest JR (1976) Mutants of Escherichia coli K-12 unable to use fumarate as an anaerobic electron acceptor. J Gen Microbiol 97:145–160
Malkhosyan SR, Rekesh AN (1985) Study of the spontaneous synthesis of colicin E1. Dokl Akad Nauk SSSR 285:492–496 (in Russian)
Malkhosyan SR, Rekesh AN (1987) Aeration affects DNA supercoiling in bacterial cells. Dokl Akad Nauk SSSR 295:1244–1247 (in Russian)
Mirkin SM. Zaitsev EN, Panyutin IG, Lyamichev VI (1984) Native supercoiling of DNA: the effects of DNA gyrase and ω protein in E. coli. Mol Gen Genet 196:508–512
Newman BM, Cole JA (1978) The chromosomal location and pleiotrophic effects of mutation of the nirA gene of Escherichia coli K-12: the essential role of nirA in nitrate reduction and in other anaerobic redox reactions. J Gen Microbiol 106:1–12
Ni Bhriain N, Dorman CF, Higgins CF (1989) An overlap between osmotic and anaerobic stress responses: a potential role for DNA supercoiling in the coordinated regulation of gene expression. Mol Microbiol 3:933–942
Novak PD, Maier RJ (1987) Inhibition of hydrogenase synthesis by DNA gyrase inhibitors in Bradyrhizobium japonicum. J Bacteriol 169:2708–2712
Overbye KM, Margolin P (1981) Role of the supX gene in ultraviolet light-induced mutagenesis in Salmonella typhimurium. J Bacteriol 146:170–178
Pruss GJ, Manes SH, Drlica K (1982) Escherichia coli DNA topoisomerase I mutants: increased supercoiling is corrected by mutations near gyrase genes. Cell 31:35–42
Pugsley AP (1984) The ins and outs of colicin. Part 1. Production and translocation across membranes. Microbiol Sci 1:168–175
Smith MW, Neidhardt FC (1983a) Proteins induced by anaerobicsis in E. coli. J Bacteriol 154:336–350
Smith MW, Neidhardt FC (1983b) Proteins induced by aerobiosis in E. coli. J Bacteriol 154:344–350
Stoker NG, Pratt JM, Holland IB (1984) In vivo gene expression system in prokaryotes. 3. The minicell system. In: Hames BD, Higgins SJ (eds) Transcription and translation. IRL Press, Oxford, pp 164–171
Vosberg H-P (1985) DNA topoisomerases: enzymes that control DNA conformation. Curr Top Microbiol Immunol 114:19–102
Wang JC (1985) DNA topoisomerases. Annu Rev Biochem 54:665–697
Yamamoto N, Droffner ML (1985) Mechanisms determining anaerobic or anaerobic growth in the facultative anaerobe Salmonella typhimurium. Proc Natl Acad Sci USA 82:2077–2081
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Malkhosyan, S.R., Panchenko, Y.A. & Rekesh, A.N. A physiological role for DNA supercoiling in the anaerobic regulation of colicin gene expression. Molec. Gen. Genet. 225, 342–345 (1991). https://doi.org/10.1007/BF00269868
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DOI: https://doi.org/10.1007/BF00269868