Skip to main content
SpringerLink
Log in

Estimating the fitness effect of an insertion sequence

  • Published:
Journal of Mathematical Biology Aims and scope Submit manuscript

Abstract

Since its discovery, mobile DNA has fascinated researchers. In particular, many researchers have debated why insertion sequences persist in prokaryote genomes and populations. While some authors think that insertion sequences persist only because of occasional beneficial effects they have on their hosts, others argue that horizontal gene transfer is strong enough to overcome their generally detrimental effects. In this study, we model the long-term fate of a prokaryote cell population, of which a small proportion of cells has been infected with one insertion sequence per cell. Based on our model and the distribution of IS5, an insertion sequence for which sufficient data is available in 525 fully sequenced proteobacterial genomes, we show that the fitness cost of insertion sequences is so small that they are effectively neutral or only slightly detrimental. We also show that an insertion sequence infection can persist and reach the empirically observed distribution if the rate of horizontal gene transfer is at least as large as the fitness cost, and that this rate is well within the rates of horizontal gene transfer observed in nature. In addition, we show that the time needed to reach the observed prevalence of IS5 is unrealistically long for the fitness cost and horizontal gene transfer rate that we computed. Occasional beneficial effects may thus have played an important role in the fast spreading of insertion sequences like IS5.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Berg DE (1989) Transposon Tn5. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, D.C., pp 185–210

    Google Scholar 

  • Bichsel M, Barbour AD, Wagner A (2010) The early phase of a bacterial insertion sequence infection. Theor Popul Biol 78: 278–288

    Article  Google Scholar 

  • Blot M (1994) Transposable elements and adaptation of host bacteria. Genetica 93(1-3): 5–12

    Article  Google Scholar 

  • Chandler M, Mahillon J (2002) Insertion sequences revisited. In: Craig NL, Craigie R, Gellert M, Lambowitz AM (eds) Mobile DNA II. American Society for Microbiology, Washington, D.C., pp 305–366

    Google Scholar 

  • Charlesworth B, Sniegowski P, Stephan W (1994) The evolutionary dynamics of repetitive DNA in eukaryotes. Nature 371: 215–219

    Article  Google Scholar 

  • Dahlberg C, Bergström M, Hermansson M (1998) In situ detection of high levels of horizontal plasmid transfer in marine bacterial communities. Appl Environ Microbiol 64(7): 2670–2675

    Google Scholar 

  • Dawkins R (1976) The selfish gene. Oxford University Press, Oxford

    Google Scholar 

  • Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284: 601–603

    Article  Google Scholar 

  • Dröge M, Pühler A, Selbitschka W (1999) Horizontal gene transfer among bacteria in terrestrial and aquatic habitats as assessed by microcosm and field studies. Biol Fertil Soils 29(3): 221–245

    Article  Google Scholar 

  • Efron B, Tibshirani RJ (1994) An introduction to the bootstrap. Chapman & Hall/CRC, New York

    Google Scholar 

  • Galas DJ, Chandler M (1989) Bacterial insertion sequences. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, D.C., pp 109–162

    Google Scholar 

  • Gibbons RJ, Kapsimalis B (1967) Estimates of the overall rate of growth of the intestinal microflora of hamsters, guinea pigs, and mice. J Bacteriol 93(1): 510–512

    Google Scholar 

  • Hall BG (1999) Transposable elements as activators of cryptic genes in E. coli. Genetica 107: 181–187

    Article  Google Scholar 

  • Jiang SC, Paul JH (1998) Gene transfer by transduction in the marine environment. Appl Environ Microbiol 64(8): 2780–2787

    Google Scholar 

  • Kleckner N (1989) Transposon Tn10. In: Berg DE, Howe MM (eds) Mobile DNA. American Society for Microbiology, Washington, D.C., pp 227–268

    Google Scholar 

  • Lan R, Reeves PR (2002) Escherichia coli in disguise: molecular origins of shigella. Microbes Infect 4(11): 1125–1132

    Article  Google Scholar 

  • Lynch M (2007) The origins of genome architecture. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Madigan MT, Martinko JM, Dunlap PV, Clark DP (2009) Brock biology of microorganisms, 12th edn. Pearson Benjamin Cummings, San Francisco

    Google Scholar 

  • Mahillon J, Siguier P, Chandler M (2009) IS Finder. http://www-is.biotoul.fr

  • NCBI (2011) National Center for Biotechnology Information. http://www.ncbi.nlm.nih.gov

  • Nelder JA, Mead R (1965) A simplex-method for function minimization. Comput J 7(4): 308–313

    Article  MATH  Google Scholar 

  • Nuzhdin SV (1999) Sure facts, speculations, and open questions about the evolution of transposable element copy number. Genetica 107: 129–137

    Article  Google Scholar 

  • Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284: 604–607

    Article  Google Scholar 

  • Savageau MA (1983) Escherichia coli habitats, cell types, and molecular mechanisms of gene control. Am Naturalist 122(6): 732–744

    Article  Google Scholar 

  • Sawyer SA, Dykhuizen DE, DuBose RF, Green L, Mutangadura-Mhlanga T, Wolczyk DF, Hartl DL (1987) Distribution and abundance of insertion sequences among natural isolates of Escherichia coli. Genetics 115: 51–63

    Google Scholar 

  • Schneider D, Lenski RE (2004) Dynamics of insertion sequence elements during experimental evolution of bacteria. Res Microbiol 155: 319–327

    Article  Google Scholar 

  • Seneta E (1981) Non-negative matrices and Markov chains. Springer, New York

    MATH  Google Scholar 

  • Shapiro JA (1999) Transposable elements as the key to a 21st century view of evolution. Genetica 107: 171–179

    Article  Google Scholar 

  • So M, McCarthy BJ (1980) Nucleotide sequence of the bacterial transposon TN1681 encoding a heat-stable (ST) toxin and its identification in enterotoxigenic Escherichia coli strains. Proc Natl Acad Sci USA 77(7): 4011–4015

    Article  Google Scholar 

  • Tavakoli NP, Derbyshire KM (2001) Tipping the balance between replicative and simple transposition. EMBO J 20(11): 2923–2930

    Article  Google Scholar 

  • Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14: 262–269

    Article  Google Scholar 

  • Touchon M, Rocha EPC (2007) Causes of insertion sequences abundance in prokaryotic genomes. Mol Biol Evol 24(4): 969–981

    Article  Google Scholar 

  • Wagner A (2006) Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes. Mol Biol Evol 23(4): 723–733

    Article  Google Scholar 

  • Wagner A, Lewis C, Bichsel M (2007) A survey of bacterial insertion sequences using IScan. Nucleic Acids Res 35(16): 5284–5293

    Article  Google Scholar 

  • Williams HG, Day MJ, Fry JC, Stewart GJ (1996) Natural transformation in river epilithon. Appl Environ Microbiol 62(8): 2994–2998

    Google Scholar 

  • Wolfram S (2003) The mathematica book, 5th edn. Wolfram Media, Champaign

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Evolutionary Biology and Environmental Studies, University of Zürich, Zuerich, Switzerland

    Manuel Bichsel & Andreas Wagner

  2. Institute of Mathematics, University of Zürich, Zuerich, Switzerland

    A. D. Barbour

Authors
  1. Manuel Bichsel
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. D. Barbour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Andreas Wagner
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manuel Bichsel.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bichsel, M., Barbour, A.D. & Wagner, A. Estimating the fitness effect of an insertion sequence. J. Math. Biol. 66, 95–114 (2013). https://doi.org/10.1007/s00285-012-0504-2

Download citation

  • Received:

  • Revised:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00285-012-0504-2

Keywords

Mathematics Subject Classification (2000)

Search

Navigation