Preferences help
enabled [disable] Abstract
Number of results
2006 | 53 | 4 | 729-738
Article title

IS1 transposition is enhanced by translation errors and by bacterial growth at extreme glucose levels

Title variants
Languages of publication
Transposition of insertion sequences (IS) is an enzyme-mediated process that only occurs in a minority of cells within a bacterial culture. Transposition is thus a rare event, but transposition frequency may vary depending on experimental conditions. For instance in a rich broth, IS elements are known to transpose during stationary phase but not during exponential growth. Using a reporter system which involves the activation of the cryptic bgl operon in Escherichia coli, we show that the frequency of IS1 transposition is a function of glucose concentration in the growth medium, it is increased by streptomycin amounts that are below minimum inhibitory concentration (sub-MIC) and is inhibited in an rpsL150 strain with high translation accuracy. Since starved cells are known to enhance ribosome frameshifting, our data suggests that growth conditions applied in this study could affect IS1 transposition by increasing translation infidelity.
Physical description
  • Plasticité et Expression des Génomes Microbiens, CNRS-FRE2383/CEA LRC12/Université Joseph Fourier, Grenoble, France
  • Plasticité et Expression des Génomes Microbiens, CNRS-FRE2383/CEA LRC12/Université Joseph Fourier, Grenoble, France
  • Plasticité et Expression des Génomes Microbiens, CNRS-FRE2383/CEA LRC12/Université Joseph Fourier, Grenoble, France
  • Plasticité et Expression des Génomes Microbiens, CNRS-FRE2383/CEA LRC12/Université Joseph Fourier, Grenoble, France
  • Plasticité et Expression des Génomes Microbiens, CNRS-FRE2383/CEA LRC12/Université Joseph Fourier, Grenoble, France
  • Atkinson J, Dodge M, Gallant J (1997) Secondary structures and starvation-induced frameshifting. Mol Microbiol 26: 747-753.
  • Barak Z, Gallant J, Linsdley D, Kwieciszewki B, Heidel D (1996) Enhanced ribosome frameshifting in stationary phase cells. J Mol Biol 263: 140-148.
  • Boe L (1992) Translational errors as the cause of mutations in Escherichia coli. Mol Gen Genet 231: 469-471.
  • Breckenridge L, Gorini L (1970) Genetic analysis of streptomycin resistance in E. coli. Genetics 65: 9-25.
  • Bull HJ, McKenzie GJ, Hastings PJ, Rosenberg SM (2000) Evidence that stationary-phase hypermutation in the Escherichia coli chromosome is promoted by recombination. Genetics 154: 1427-1437.
  • Casadaban MJ (1976) Transposition and fusion of the lac genes to selected promoters in Escherichia coli using bacteriophage lambda and Mu. J Mol Biol 104: 541-555.
  • Cashel M, Gentry DR, Hernandez VJ, Vinella D (1996) The stringent response. In Escherichia coli and Salmonella typhimurium Cellular and Molecular Biology (Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE, eds), pp 1458-1496. American Society of Microbiology, Washington DC.
  • Chalmers R, Blot M (1999) Insertion sequences and transposons In Organisation of the Procaryotic Genome (Charlebois RL ed) pp 151-169. ASM Press, NY.
  • Chao L, McBroom SM (1985) Evolution of transposable elements: an IS10 insertion increases fitness in Escherichia coli. Mol Biol Evol 2: 359-369.
  • Chao L, Vargas C, Spear BB, Cox EC (1983) Transposable elements as mutator genes in evolution. Nature 303: 633-635.
  • Cooper VS, Schneider D, Blot M, Lenski RE (2001) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. J Bacteriol 183: 2834-2841.
  • Defez R, De Felice M (1981) Cryptic operon for β-glucoside metabolism in Escherichia coli K12: genetic evidence for a regulatory protein. Genetics 97: 11-25.
  • Di Nardo S, 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.
  • Escoubas JM, Prère MF, Fayet O, Salvignol I, Galas D, Zerbib D, Chandler M (1991) Translational control of transposition activity of the bacterial insertion sequence IS1. EMBO J 10: 705-712.
  • Escoubas JM, Lane D, Chandler M (1994) Is the IS1 transposase, InsAB', the only IS1-encoded protein required for efficient transposition? J Bacteriol 176: 5864-5867.
  • Flardh K, Axeberg T, Albertson NH, Kjelleberg S (1994) Stringent control during carbon starvation of marine Vibrio sp. strain S14: molecular cloning, nucleotide sequence, and deletion of the relA gene. J Bacteriol 176: 5949-5957.
  • Funtasu G, Nierhaus K, Wittman HG (1972) Determination of allele types and amino-acid exchanges in protein S12 of 3 streptomycin-resistant mutants of E. coli. Biochim Biophys Acta 287: 282-291.
  • Gentry DR, Cashel M (1996) Mutational analysis of the Escherichia coli spoT gene identifies distinct but overlapping regions involved in ppGpp synthesis and degradation. Mol Microbiol 19: 1373-1384.
  • Giel M, Desnoyer M, Lopilato J (1996) A mutation in a new gene, bglJ, activate the bgl operon in Escherichia coli-K12. Genetics 143: 627-635.
  • Gorini L (1971) Streptomycin and misreading of the genetic code. In Ribosomes (Nomura M, Tissièress A, Lengyel P, eds) pp 791-803. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
  • Hall BG (1998) Activation of the bgl operon by adaptive mutation. Mol Biol Evol 15: 1-5.
  • Hall BG (1999a) Spectra of spontaneous growth-dependent and adaptive mutations at ebgR. J Bacteriol 181: 1149-1155.
  • Hall BG (1999b) Transposable elements as activators of cryptic genes in E. coli. Genetica 107: 181-187.
  • Hernandez VJ, Bremer H (1991) Escherichia coli ppGpp synthetase II activity requires spoT. J Biol Chem 266: 5991-5999.
  • Kurland CG (1992) Translational accuracy and the fitness of bacteria. Ann Rev Genet 26: 29-50.
  • Lea DE, Coulson CA (1949) The distribution of the numbers of mutants in bacterial populations. J Genet 49: 264-285.
  • Levin BR, Perrot V, Walker N (2000) Compensatory mutations, antibiotic resistance and the population genetics of adaptative evolution in bacteria. Genetics 154: 985-997.
  • Mahillon J, Chandler M (1998) Insertion sequences. Microbiol Mol Biol Rev 62: 725-774.
  • Mikkola R, Kurland CG (1992) Selection of laboratory wild-type phenotype from natural isolates of Escherichia coli in chemostats. Mol Biol Evol 9: 394-402.
  • Moorthy S, Mahadevan S (2002) Differential spectrum of mutations that activate the Escherichia coli bgl operon in an rpoS genetic background. J Bacteriol 184: 4033-4038.
  • Murray DK, Bremer H (1996) Control of spoT-dependent ppGpp synthesis and degradation in Escherichia coli. J Biol Chem 259: 41-57.
  • Orgel LE, Crick FH (1980) Selfish DNA: the ultimate parasite. Nature 284: 604-607.
  • Parker J (1989) Errors and alternatives in reading the universal genetic code. Microbiol Rev 53: 273-298.
  • Post LE, Nomura M (1980) DNA sequences from the str operon of Escherichia coli. J Biol Chem 255: 4660-4666.
  • Reynolds AE, Felton J, Wright A (1981) Insertion of DNA activates the cryptic bgl operon in E. coli K12. Nature 293: 625-629.
  • Rodriguez H, Snow ET, Bhat U, Loechler EL (1992) An Escherichia coli plasmid-based, mutational system in which supF mutants are selectable - insertion elements dominate the spontaneous spectra. Mutat Res 270: 219-231.
  • Ruusala T, Kurland CG (1984) Streptomycin preferentially perturbs ribosomal proofreading. Mol Gen Genet 198: 100-104.
  • Ruusala T, Andersson D, Ehrenberg M, Kurland CG (1984) Hyper-accurate ribosomes inhibit growth. EMBO J 3: 2575-2580.
  • Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press.
  • Schneider D, Faure D, Noirclerc-Savoye M, Coursange E, Blot M (2000) A broad-host range plasmid to isolate mobile genetic elements in gram negative bacteria. Plasmid 44: 201-207.
  • Schneider D, Duperchy E, Coursange E, Lenski RE, Blot M (2001) Long-term experimental evolution in Escherichia coli. IX. Characterization of insertion sequence-mediated mutations and rearrangements. Genetics 156: 477-488.
  • Schnetz K, Rak B (1992) IS5 - a mobile enhancer of transcription in Escherichia coli. Proc Natl Acad Sci USA 89: 1244-1248.
  • Schnetz K, Toloczyki C, Rak B (1987) β-Glucosides (bgl) operon of Escherichia coli K-12: nucleotide sequence, genetic organization, and possible evolutionary relationship to regulatory components to two Bacillus subtilis genes. J Bacteriol 169: 2579-2590.
  • Sekine Y, Ohtsubo E (1989) Frameshifting is required for production of the transposase encoded by insertion sequence 1. Proc Natl Acad Sci USA 86: 4609-4613.
  • Shiga Y, Sekine Y, Kano Y, Ohtsubo E (2001) Involvement of H-NS in transpositional recombination mediated by IS1. J Bacteriol 183: 2476-2484.
  • Treves DS, Manning S, Adams J (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15: 789-797.
  • Ueguchi C, Ohta T, Set C, Suzuku T, Mizuno T (1998) The leuO gene product has a latent ability to relieve bgl silencing in E. coli. J Bacteriol 180: 190-193.
  • Xiao H, Kalman M, Ikehara K, Zemel S, Glaser G, Cashel M (1991) Residual guanosine 3',5'-bispyrophosphate synthetic activity of relA null mutants can be eliminated by Spot null mutations. J Biol Chem 266: 5980-5990.
Document Type
Publication order reference
YADDA identifier
JavaScript is turned off in your web browser. Turn it on to take full advantage of this site, then refresh the page.