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. 1983 Apr;103(4):581–592. doi: 10.1093/genetics/103.4.581

Evolution of Transposons: Natural Selection for Tn5 in ESCHERICHIA COLI K12

Susan Wurster Biel 1,2, Daniel L Hartl 1,2
PMCID: PMC1202041  PMID: 6303898

Abstract

A novel in vivo effect of the transposable element Tn 5 has been observed in chemostats when certain isogenic Tn5 and non-Tn5 strains of Escherichia coli compete for a limiting carbon source in the absence of kanamycin. The Tn5-bearing strain has a more rapid growth rate and increases in frequency from 50% to 90% within the first 15 to 20 generations. The effect occurs when Tn5 is inserted at a variety of chromosomal locations or when the element is carried by an episome, but it is strain specific, having been observed in two out of three strains examined. (For reasons unknown, the effect has not been observed with derivatives of strain CSH12.) Although the growth-rate advantage of Tn 5 is independent of nutrient concentration and generation time, it can be reduced by prior adaptation of the strains to limiting conditions, and the amount of reduction is proportional to the length of prior adaptation. The growth-rate effect is evidently not caused by beneficial mutations induced by Tn5 transposition, as Tn5-bearing strains selected in chemostats retain their initial Tn5 position and copy number. However, the effect does not occur in Tn5-112, a transpositionless deletion mutation missing the transposase-coding region of the right-hand IS sequence flanking the element. Since Tn5-112 retains a functional kanamycin-phosphotransferase gene, this gene is not responsible for the growth-rate effect. Thus, the effect evidently requires transposase function, but it does not involve actual transposition of the intact element. Altogether, these data provide a mechanism for the maintenance of Tn5 in bacterial populations in the absence of kanamycin, and they suggest a model for the proliferation and the maintenance of IS sequences and transposable elements in the absence of other identifiable selection pressures.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Anderson E. S. The ecology of transferable drug resistance in the enterobacteria. Annu Rev Microbiol. 1968;22:131–180. doi: 10.1146/annurev.mi.22.100168.001023. [DOI] [PubMed] [Google Scholar]
  2. Berg D. E. Control of gene expression by a mobile recombinational switch. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4880–4884. doi: 10.1073/pnas.77.8.4880. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Berg D. E., Davies J., Allet B., Rochaix J. D. Transposition of R factor genes to bacteriophage lambda. Proc Natl Acad Sci U S A. 1975 Sep;72(9):3628–3632. doi: 10.1073/pnas.72.9.3628. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berg D. E., Drummond M. Absence of DNA sequences homologous to transposable element Tn5 (Kan) in the chromosome of Escherichia coli K-12. J Bacteriol. 1978 Oct;136(1):419–422. doi: 10.1128/jb.136.1.419-422.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Berg D. E., Johnsrud L., McDivitt L., Ramabhadran R., Hirschel B. J. Inverted repeats of Tn5 are transposable elements. Proc Natl Acad Sci U S A. 1982 Apr;79(8):2632–2635. doi: 10.1073/pnas.79.8.2632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Calos M. P., Miller J. H. Transposable elements. Cell. 1980 Jul;20(3):579–595. doi: 10.1016/0092-8674(80)90305-0. [DOI] [PubMed] [Google Scholar]
  7. Campbell A., Berg D. E., Botstein D., Lederberg E. M., Novick R. P., Starlinger P., Szybalski W. Nomenclature of transposable elements in prokaryotes. Gene. 1979 Mar;5(3):197–206. doi: 10.1016/0378-1119(79)90078-7. [DOI] [PubMed] [Google Scholar]
  8. Doolittle W. F., Sapienza C. Selfish genes, the phenotype paradigm and genome evolution. Nature. 1980 Apr 17;284(5757):601–603. doi: 10.1038/284601a0. [DOI] [PubMed] [Google Scholar]
  9. KUBITSCHEK H. E., BENDIGKEIT H. E. MUTATION IN CONTINUOUS CULTURES. I. DEPENDENCE OF MUTATIONAL RESPONSE UPON GROWTH-LIMITING FACTORS. Mutat Res. 1964 Jul;106:113–120. doi: 10.1016/0027-5107(64)90013-2. [DOI] [PubMed] [Google Scholar]
  10. Lin L., Bitner R., Edlin G. Increased reproductive fitness of Escherichia coli lambda lysogens. J Virol. 1977 Feb;21(2):554–559. doi: 10.1128/jvi.21.2.554-559.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Rothstein S. J., Jorgensen R. A., Postle K., Reznikoff W. S. The inverted repeats of Tn5 are functionally different. Cell. 1980 Mar;19(3):795–805. doi: 10.1016/s0092-8674(80)80055-9. [DOI] [PubMed] [Google Scholar]
  12. Rubens C. E., Farrar W. E., Jr, McGee Z. A., Schaffner W. Evolution of a plasmid mediating resistance to multiple antimicrobial agents during a prolonged epidemic of nosocomial infections. J Infect Dis. 1981 Feb;143(2):170–181. doi: 10.1093/infdis/143.2.170. [DOI] [PubMed] [Google Scholar]
  13. Saedler H., Cornelis G., Cullum J., Schumacher B., Sommer H. IS1-mediated DNA rearrangements. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):93–98. doi: 10.1101/sqb.1981.045.01.017. [DOI] [PubMed] [Google Scholar]
  14. Sapienza C., Doolittle W. F. Genes are things you have whether you want them or not. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 1):177–182. doi: 10.1101/sqb.1981.045.01.028. [DOI] [PubMed] [Google Scholar]
  15. Selander R. K., Levin B. R. Genetic diversity and structure in Escherichia coli populations. Science. 1980 Oct 31;210(4469):545–547. doi: 10.1126/science.6999623. [DOI] [PubMed] [Google Scholar]
  16. Smith J. M., Smolin D. E., Umbarger H. E. Polarity and the regulation of the ilv gene cluster in Escherichia coli strain K-12. Mol Gen Genet. 1976 Oct 18;148(2):111–124. doi: 10.1007/BF00268374. [DOI] [PubMed] [Google Scholar]
  17. Watson M. D., Wild J., Umbarger H. E. Positive control of ilvC expression in Escherichia coli K-12; identification and mapping of regulatory gene ilvY. J Bacteriol. 1979 Sep;139(3):1014–1020. doi: 10.1128/jb.139.3.1014-1020.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]

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