Skip to main content
Log in

Unusual codon bias occurring within insertion sequences in Escherichia coli

  • Research Article
  • Published:
Genetica Aims and scope Submit manuscript

Abstract

The large open reading frames of insertion sequences from Escherichia coli were examined for their spatial pattern of codon usage bias and distribution of rarely used codons. There is a bias in codon usage that is generally lower toward the terminal ends of the coding regions, which is reflected in the occurrence of an excess of nonpreferred codons in the 3′ portions of the coding regions as compared with the 5′ portions. In contrast, typical chromosomal genes have a lower codon usage bias toward the 5′ ends of the coding regions. These results imply that the selective forces reflected in codon usage bias may differ according to position within the coding sequence. In addition, these constraints apparently differ in important ways between genes contained in insertion sequences and those in the chromosome.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ayer, D. & Yarus, M., 1986. The context effect does not require a fourth base pair. Science 231: 393–395.

    Google Scholar 

  • Bennetzen, J. L. & Hall, B. D., 1982. Codon selection in yeast. J. Biol. Chem. 257: 3026–3031.

    Google Scholar 

  • Bulmer, M., 1988. Codon usage and intragenic position. J. Theor. Biol. 133: 67–71.

    Google Scholar 

  • Blundell, M., Craig, E. & Kennell, D., 1972. Decay rates of different mRNA in E. coli and models of decay. Nature New Biol. 238: 46–49.

    Google Scholar 

  • Bonekamp, F., Andersen, H. D., Christensen, T. & Jensen, K. F., 1985. Codon-defined ribosomal pausing detected by using the pyrE attenuator to probe the coupling between transcription and translation. Nuc. Acids Res. 13: 4113–4123.

    Google Scholar 

  • Bossi, L., 1983. Context effects: Translation of UAG codon by suppressor tRNA is affected by the sequence following UAG in the message. J. Mol. Biol. 164: 73–87.

    Google Scholar 

  • Bossi, L. & Roth, J. R., 1980. The influence of codon context on genetic code translation. Nature 286: 123–127.

    Google Scholar 

  • Burns, D. M. & Beacham, I. R., 1985. Rare codons in E. coli and S. typhimurium signal sequences. FEBS Lett. 189: 318–324.

    Google Scholar 

  • Cannistraro, V. J., Subbarao, M. N. & Kennell, D., 1986. Specific endonucleolytic cleavage sites for decay of Escherichia coli mRNA. J. Mol. Biol. 192: 257–274.

    Google Scholar 

  • Carter, P. W., Bartkus, J. M. & Calvo, J. M., 1986. Transcription attenuation in Salmonella typhimurium: the significance of rare leucine codons in the leu leader. Proc. Nat. Acad. Sci., USA 83: 8127–8131.

    Google Scholar 

  • Dix, D. B. & Thompson, R. C., 1989. Codon choice and gene expression: Synonymous codons differ in translational accuracy. Proc. Nat. Acad. Sci., USA 86: 6888–6892.

    Google Scholar 

  • Galas, D. J. & Chandler, M., 1989. Bacterial Insertion Sequences, pp. 109–162 in Mobile DNA, edited by D. E.Berg and M. M.Howe. American Society for Microbiology, Washington, D.C.

    Google Scholar 

  • Grindley, N. D. F. & Joyce, C. M., 1981. Analysis of the structure and function of the kanamycin-resistance transposon Tn903. Cold Spring Harb. Symp. Quant. Biol. 45: 125–133.

    Google Scholar 

  • Gouy, M. & Gautier, C., 1982. Codon usage in bacteria: correlation with gene expressivity. Nuc. Acids Res. 10: 7055–7074.

    Google Scholar 

  • Gutman, G. A. & Hatfield, G. W., 1989. Nonrandom utilization of codon pairs in Escherichia coli. Proc. Nat. Acad. Sci., USA 86: 3699–3703.

    Google Scholar 

  • Harms, E. & Umbarger, H. E., 1987. Role of codon choice in the leader region of the ilvGMEAA operon of Serratia marcescens. J. Bacteriol. 169: 5668–5677.

    Google Scholar 

  • Holm, L., 1986. Codon usage and gene expression. Nuc. Acids Res. 14: 3075–3087.

    Google Scholar 

  • Ikemura, T., 1981. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J. Mol. Biol. 146: 1–21.

    Google Scholar 

  • Ikemura, T., 1985. Codon usage and tRNA content in unicellular and multicellular organisms. Mol. Biol. Evol. 2: 13–34.

    Google Scholar 

  • Jack, H. M., Berg, J. & Wahl, M., 1987. Translation affects immunoglobulin mRNA stability. Eur. J. Immunol. 19: 843–847.

    Google Scholar 

  • Kennell, D. E., 1986. The instability of messenger RNA in bacteria, pp. 101–142 in Maximizing Gene Expression, edited by W. S.Reznikoff and L.Gold. Butterworths, Stoneham, MA.

    Google Scholar 

  • Kepes, A., 1967. Sequential transcription and translation in the lactose operon of Escherichia coli. Biochim. Biophys. Acta 138: 107–123.

    Google Scholar 

  • Levinthal, C., Fan, D. P., Higa, A. & Zimmermann, R. A., 1963. The decay and protection of messenger RNA in bacteria. Cold Spring Harb. Symp. Quant. Biol. 28: 183–190.

    Google Scholar 

  • Lijenström, H. & VonHeijne, G., 1987. Translation rate modification by preferential codon usage: intragenic position effects. J. Theor. Biol. 124: 43–55.

    Google Scholar 

  • Machida, Y., Machida, C., Ohtsubo, H. & Ohtsubo, E., 1982. Factors determining frequency of plasmid cointegration mediated by insertion sequence IS1. Proc. Nat. Acad. Sci., USA 79: 277–281.

    Google Scholar 

  • Misra, S. & Rio, C., 1990. Cytotype control of Drosophila P element transposition: The 66 kd protein is a repressor of transposase activity. Cell 40: 269–284.

    Google Scholar 

  • Morisato, D., Way, J. C., Kim, H.-J. & Kleckner, N., 1983. Tn10 transposase acts preferentially on nearby transposon ends in vivo. Cell 32: 799–807.

    Google Scholar 

  • Morse, D. E. & Yanosfky, C., 1969. Polarity and the degradation of mRNA. Nature 224: 329–331.

    Google Scholar 

  • Petersen, C., 1987. The functional stability of the lacZ transcript is sensitive towards sequence alterations immediately downstream of the ribosome binding site. Mol. Gen. Genet. 209: 179–187.

    Google Scholar 

  • Reimmann, C., Moore, R., Little, S., Savioz, A., Willetts, N. S. & Haas, D., 1989. Genetic structure, function, and regulation of the transposable element IS21. Mol. Gen. Genet. 214: 416–424.

    Google Scholar 

  • Robinson, M., Lilley, R., Little, S., Emtage, J. S., Yarranton, G., Stephens, P., Millican, A., Eaton, M. & Humphreys, G., 1984. Codon usage can affect efficiency of translation of genes in Escherichia coli. Nuc. Acids Res. 12: 6663–6671.

    Google Scholar 

  • Sawyer, S. A., Dykhuizen, D. E., DuBose, R. F., Green, L., Mutangadura-Mhlanga, T., Wolczyk, D. F. & Hartl, D. L., 1987. Distribution and abundance of insertion sequences among natural isolates of Escherichia coli. Genetics 115: 51–63.

    Google Scholar 

  • Sekine, Y. & Ohtsubo, E., 1989. Frameshifting is required for production of the transposase encoded by insertion sequence 1. Proc. Nat. Acad. Sci., USA 86: 4609–4613.

    Google Scholar 

  • Sharp, P. M. & Li, W. H., 1986. Codon usage in regulatory genes in Escherichia coli do not reflect selection for ‘rare’ codons. Nuc. Acids Res. 14: 7737–7749.

    Google Scholar 

  • Sharp, P. M. & Li, W. H., 1987a. Rate of synonymous substitution in Enterobacterial genes in inversely related to codon usage bias. Mol. Biol. Evol. 4: 222–230.

    Google Scholar 

  • Sharp, P. M. & Li, W. H., 1987b. The codon adaptation index—a measure of directional synonymous codon usage bias, and its potential applications. Nuc. Acids Res. 15: 1281–1295.

    Google Scholar 

  • Sharp, P. M., Cowe, E., Higgins, D. G., Shields, D. C., Wolfe, K. H. & Wright, F., 1988. Codon usage patterns in Escherichia coli, Bacillus subtilus, Saccharomyces cerevisiae, Schizosaccha romyces pombe, Drosophila melanogaster, and Homo sapiens; a review of the considerable within species diversity. Nuc. Acids Res. 16: 8207–8211.

    Google Scholar 

  • Stadler, R., Caspers, P., Olasz, F. & Arber, W., 1990. The N-terminal domain of the insertion sequence 30 transposase interacts specifically with the terminal inverted repeats of the element. J. Biol. Chem. 265: 3757–3762.

    Google Scholar 

  • Thompson, R. C., Dix, D. B. & Eccleston, J. F., 1980. Single tunover kinetic studies of guanosine triphosphate hydrolysis and peptide formation in the elongation factor Tu dependent binding of aminoacyl-tRNA to Escherichia coli ribosomes. J. Biol. Chem. 255: 11088–11090.

    Google Scholar 

  • vonGabain, A., Belasco, J. G., Schottel, J. C., Chang, A. C. Y. & Cohen, S. N., 1983. Decay of mRNA in Escherichia coli: Investigation of the fate of specific segments of transcripts. Proc. Nat. Acad. Sci., USA 80: 653–657.

    Google Scholar 

  • Wikström, P. M. & Björk, G. R., 1989. A regulatory element within a gene of a ribosomal protein operon of Escherichia coli negatively controls expression by decreasing the translational efficiency. Mol. Gen. Genet. 219: 381–389.

    Google Scholar 

  • Varenne, S., Buc, J., Lloubes, R. & Lazdunski, C., 1984. Translation is a non-uniform process: effect of tRNA availability on the rate of elongation of nascent polypeptide chains. J. Mol. Biol. 180: 549–576.

    Google Scholar 

  • Yarus, M., 1979. The accuracy of translation. Prog. Nuc. Acid Res. Mol. Biol. 23: 195–225.

    Google Scholar 

  • Yarus, M., & Folley, L. S., 1985. Sense codons are found in specific contexts. J. Mol. Biol. 182: 529–540.

    Google Scholar 

  • Zerbib, D., Jakowec, M., Prentki, P., Galas, D. & Chandler, M., 1987. Expression of proteins essential for IS1 transposition: specific binding of InsA to the ends of IS1. EMBO J. 6: 3163–3169.

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Lawrence, J.G., Hartl, D.L. Unusual codon bias occurring within insertion sequences in Escherichia coli . Genetica 84, 23–29 (1991). https://doi.org/10.1007/BF00123981

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00123981

Keywords

Navigation