Skip to main content
Log in

Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli

  • Published:
Genetica Aims and scope Submit manuscript

Abstract

Insertion sequences (ISs) are transposable genetic elements in bacterial genomes. IS elements are common among bacteria but are generally rare within free-living species, probably because of the negative fitness effects they have on their hosts. Conversely, ISs frequently proliferate in intracellular symbionts and pathogens that recently transitioned from a free-living lifestyle. IS elements can profoundly influence the genomic evolution of their bacterial hosts, although it is unknown why they often expand in intracellular bacteria. We designed a laboratory evolution experiment with Escherichia coli K-12 to test the hypotheses that IS elements often expand in intracellular bacteria because of relaxed natural selection due to (1) their generally small effective population sizes (N e) and thus enhanced genetic drift, and (2) their nutrient rich environment, which makes many biosynthetic genes unnecessary and thus selectively neutral territory for IS insertion. We propagated 12 populations under four experimental conditions: large N e versus small N e, and nutrient rich medium versus minimal medium. We found that relaxed selection over 4,000 generations was not sufficient to permit IS element expansion in any experimental population, thus leading us to hypothesize that IS expansion in intracellular symbionts may often be spurred by enhanced transposition rates, possibly due to environmental stress, coupled with relaxed natural selection.

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.

Fig. 1

Similar content being viewed by others

References

  • Bergthorsson U, Ochman H (1995) Heterogeneity of genome sizes among natural isolates of Escherichia coli. J Bacteriol 177:5784–5789

    PubMed  CAS  Google Scholar 

  • Bergthorsson U, Ochman H (1998) Distribution of chromosome length variation in natural isolates of Escherichia coli. Mol Biol Evol 15:6–16

    PubMed  CAS  Google Scholar 

  • Blattner FR, Plunkett G, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462

    Article  PubMed  CAS  Google Scholar 

  • Brinster S, Lamberet G, Staels B, Trieu-Cuot P, Gruss A, Poyart C (2009) Type II fatty acid synthesis is not a suitable antibiotic target for Gram-positive pathogens. Nature 458:83–86

    Article  PubMed  CAS  Google Scholar 

  • Capy P, Gasperi G, Biémont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85:101–106

    Article  PubMed  CAS  Google Scholar 

  • Chain PSG, Hu P, Malfatti SA, Radnedge L, Larimer F, Vergez LM, Worsham P, Chu MC, Andersen GL (2006) Complete genome sequence of Yersinia pestis strains Antiqua and Nepal516: evidence of gene reduction in an emerging pathogen. J Bacteriol 188:4453–4463

    Article  PubMed  Google Scholar 

  • Chandler M, Mahillon J (2002) Insertion sequences revisited. In: Craig NL, Craigie R, Gellert M, Lambowitz A (eds) Mobile DNA II, vol 5/6. ASM Press, Washington, pp 305–366

    Google Scholar 

  • Chao L, McBroom SM (1985) Evolution of transposable elements: an IS10 insertion increases fitness in Escherichia coli. Mol Biol Evol 2:359–369

    PubMed  CAS  Google Scholar 

  • Conlon KM, Humphreys H, O’Gara JP (2004) Inactivations of rsbU and sarA by IS256 represent novel mechanisms of biofilm phenotypic variation in Staphylococcus epidermidis. J Bacteriol 186:6208–6219

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Cornelis G (1980) Transposition of Tn951 (Tnlac) and cointegrate formation are thermosensitive processes. J Gen Microbiol 117:243–247

    PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Dougherty KM, Plague GR (2008) Transposable element loads in a bacterial symbiont of weevils are extremely variable. Appl Environ Microbiol 74:7832–7834

    Article  PubMed  CAS  Google Scholar 

  • Duchaud E, Rusniok C, Frangeul L, Buchrieser C, Taourit S, Bocs S, Boursaux-Eude C, Chandler M, Dassa E, Derose R, Derzelle S, Freyssinet G, Gaudriault S, Givaudan A, Médigue C, Lanois A, Powell K, Siguier P, Wingate V, Zouine M, Glaser P, Boemare N, Danchin A, Kunst F (2003) The genome sequence of the entomopathogenic bacterium Photorhabdus luminescens. Nat Biotechnol 21:1307–1313

    Article  PubMed  CAS  Google Scholar 

  • Dykhuizen DE (1990) Experimental studies of natural selection in bacteria. Annu Rev Ecol Syst 21:373–398

    Article  Google Scholar 

  • Edwards RJ, Brookfield JFY (2003) Transiently beneficial insertions could maintain mobile DNA sequences in variable environments. Mol Biol Evol 20:30–37

    Article  PubMed  CAS  Google Scholar 

  • Elena SF, Ekunwe L, Hajela N, Oden SA, Lenski RE (1998) Distribution of fitness effects caused by random insertion mutations in Escherichia coli. Genetica 102(103):349–358

    Article  PubMed  Google Scholar 

  • Fraser C, Hanage WP, Spratt BG (2007) Recombination and the nature of bacterial speciation. Science 315:476–480

    Article  PubMed  CAS  Google Scholar 

  • Haren L, Bétermier M, Polard P, Chandler M (1997) IS911-mediated intramolecular transposition is naturally temperature sensitive. Mol Microbiol 25:531–540

    Article  PubMed  CAS  Google Scholar 

  • Herzer PJ, Inouye S, Inouye M, Whittam TS (1990) Phylogenetic distribution of branched RNA-linked multicopy single-stranded DNA among natural isolates of Escherichia coli. J Bacteriol 172:6175–6181

    PubMed  CAS  Google Scholar 

  • Kang Y, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR (2004) Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186:4921–4930

    Article  PubMed  CAS  Google Scholar 

  • Kimura M (1983) The neutral theory of molecular evolution. Cambridge University Press, Cambridge

    Google Scholar 

  • Kimura M, Ohta T (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 61:763–771

    PubMed  CAS  Google Scholar 

  • Kothary MH, Babu US (2001) Infective dose of foodborne pathogens in volunteers: a review. J Food Saf 21:49–73

    Article  Google Scholar 

  • Kretschmer PJ, Cohen SN (1979) Effect of temperature on translocation frequency of the Tn3 element. J Bacteriol 139:515–519

    PubMed  CAS  Google Scholar 

  • Leavis HL, Willems RJL, van Wamel WJB, Schuren FH, Caspers MPM, Bonten MJM (2007) Insertion sequence-driven diversification creates a globally dispersed emerging multiresistant subspecies of E. faecium. PLoS Pathog 3:e7

    Article  PubMed  Google Scholar 

  • Lederberg J (2004) E. coli K-12. Microbiol Today 31:116

    Google Scholar 

  • Lee B-M, Park Y-J, Park D-S, Kang H-W, Kim J-G, Song E-S, Park I-C, Yoon U-H, Hahn J-H, Koo B-S, Lee G-B, Kim H, Park H-S, Yoon K-O, Kim J-H, Jung C-h, Koh N-H, Seo J-S, Go S-J (2005) The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Res 33:577–586

    Article  PubMed  CAS  Google Scholar 

  • Lenski RE, Rose MR, Simpson SC, Tadler SC (1991) Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am Nat 138:1315–1341

    Article  Google Scholar 

  • Lind PA, Berg OG, Andersson DI (2010) Mutational robustness of ribosomal protein genes. Science 330:825–827

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Lynch M, Conery JS (2003) The origins of genome complexity. Science 302:1401–1404

    Article  PubMed  CAS  Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor

    Google Scholar 

  • Moran NA, Plague GR (2004) Genomic changes following host restriction in bacteria. Curr Opin Genet Dev 14:627–633

    Article  PubMed  CAS  Google Scholar 

  • Moran NA, Wernegreen JJ (2000) Lifestyle evolution in symbiotic bacteria: insights from genomics. Trends Ecol Evol 15:321–326

    Article  PubMed  Google Scholar 

  • Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119:736–747

    PubMed  CAS  Google Scholar 

  • Newton ILG, Bordenstein SR (2011) Correlations between bacterial ecology and mobile DNA. Curr Microbiol 62:198–208

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Davalos LM (2006) The nature and dynamics of bacterial genomes. Science 311:1730–1733

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Moran NA (2001) Genes lost and genes found: evolution of bacterial pathogenesis and symbiosis. Science 292:1096–1098

    Article  PubMed  CAS  Google Scholar 

  • Ochman H, Wilson AC (1987) Evolutionary history of enteric bacteria. In: Neidhardt FC, Ingraham JL, Low KB, Magasanik B, Schaechter M, Umbarger HE (eds) Escherichia coli and Salmonella typhimurium: cellular and molecular biology. ASM Press, Washington, pp 1649–1654

    Google Scholar 

  • Ohta T (1973) Slightly deleterious mutant substitutions in evolution. Nature 246:96–98

    Article  PubMed  CAS  Google Scholar 

  • Ohtsubo Y, Genka H, Komatsu H, Nagata Y, Tsuda M (2005) High-temperature-induced transposition of insertion elements in Burkholderia multivorans ATCC 17616. Appl Environ Microbiol 71:1822–1828

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Papadopoulos D, Schneider D, Meier-Eiss J, Arber W, Lenski RE, Blot M (1999) Genomic evolution during a 10,000-generation experiment with bacteria. Proc Natl Acad Sci USA 96:3807–3812

    Article  PubMed  CAS  Google Scholar 

  • Parkhill J, Sebaihia M, Preston A, Murphy LD, Thomson N, Harris DE, Holden MT, Churcher CM, Bentley SD, Mungall KL, Cerdeño-Tarraga AM, Temple L, James K, Harris B, Quail MA, Achtman M, Atkin R, Baker S, Basham D, Bason N, Cherevach I, Chillingworth T, Collins M, Cronin A, Davis P, Doggett J, Feltwell T, Goble A, Hamlin N, Hauser H, Holroyd S, Jagels K, Leather S, Moule S, Norberczak H, O’Neil S, Ormond D, Price C, Rabbinowitsch E, Rutter S, Sanders M, Saunders D, Seeger K, Sharp S, Simmonds M, Skelton J, Squares R, Squares S, Stevens K, Unwin L, Whitehead S, Barrell BG, Maskell DJ (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40

    Article  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:2002–2007

    Article  Google Scholar 

  • Pfaffl MW (2004) Quantification strategies in real-time PCR. In: Bustin SA (ed) A-Z of quantitative PCR, vol 2–3. International University Line Press, La Jolla, pp 87–120

    Google Scholar 

  • Pfeifer F, Blaseio U (1990) Transposition burst of the ISH27 insertion element family in Halobacterium halobium. Nucleic Acids Res 18:6921–6925

    Article  PubMed  CAS  Google Scholar 

  • Plague GR, Dunbar HE, Tran PL, Moran NA (2008) Extensive proliferation of transposable elements in heritable bacterial symbionts. J Bacteriol 190:777–779

    Article  PubMed  CAS  Google Scholar 

  • Riley M (1993) Functions of the gene products of Escherichia coli. Microbiol Rev 57:862–952

    PubMed  CAS  Google Scholar 

  • Russell DG (2005) Where to stay inside the cell: a homesteader’s guide to intracellular parasitism. In: Cossart P, Boquet P, Normark S, Rappuoli R (eds) Cellular microbiology, 2nd edn. ASM Press, Washington, pp 227–253

    Google Scholar 

  • Safi H, Barnes PF, Lakey DL, Shams H, Samten B, Vankayalapati R, Howard ST (2004) IS6110 functions as a mobile, monocyte-activated promoter in Mycobacterium tuberculosis. Mol Microbiol 52:999–1012

    Article  PubMed  CAS  Google Scholar 

  • Schmitz-Esser S, Tischler P, Arnold R, Montanaro J, Wagner M, Rattei T, Horn M (2010) The genome of the amoeba symbiont “Candidatus Amoebophilus asiaticus” reveals common mechanisms for host cell interaction among amoeba-associated bacteria. J Bacteriol 192:1045–1057

    Article  PubMed  CAS  Google Scholar 

  • Song Y, Tong Z, Wang J, Wang L, Guo Z, Han Y, Zhang J, Pei D, Zhou D, Qin H, Pang X, Han Y, Zhai J, Li M, Cui B, Qi Z, Jin L, Dai R, Chen F, Li S, Ye C, Du Z, Lin W, Wang J, Yu J, Yang H, Wang J, Huang P, Yang R (2004) Complete genome sequence of Yersinia pestis strain 91001, an isolate avirulent to humans. DNA Res 11:179–197

    Article  PubMed  CAS  Google Scholar 

  • Todd ECD, Greig JD, Bartleson CA, Michaels BS (2008) Outbreaks where food workers have been implicated in the spread of foodborne disease. Part 4. Infective doses and pathogen carriage. J Food Prot 71:2339–2373

    PubMed  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • Wahl LM, Gerrish PJ (2001) The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55:2606–2610

    PubMed  CAS  Google Scholar 

  • Whittam TS, Ake SE (1993) Genetic polymorphisms and recombination in natural populations of Escherichia coli. In: Takahata N, Clark AG (eds) Mechanisms of molecular evolution. Sinauer Associates, Sunderland, pp 223–245

    Google Scholar 

  • Woyke T, Teeling H, Ivanova NN, Huntemann Ml, Richter M, Gloeckner FO, Boffelli D, Anderson IJ, Barry KW, Shapiro HJ, Szeto E, Kyrpides NC, Mussmann M, Amann R, Bergin C, Ruehland C, Rubin EM, Dubilier N (2006) Symbiosis insights through metagenomic analysis of a microbial consortium. Nature 443:950–955

    Article  PubMed  CAS  Google Scholar 

  • Yang F, Yang J, Zhang X, Chen L, Jiang Y, Yan Y, Tang X, Wang J, Xiong Z, Dong J, Xue Y, Zhu Y, Xu X, Sun L, Chen S, Nie H, Peng J, Xu J, Wang Y, Yuan Z, Wen Y, Yao Z, Shen Y, Qiang B, Hou Y, Yu J, Jin Q (2005) Genome dynamics and diversity of Shigella species, the etiologic agents of bacillary dysentery. Nucleic Acids Res 33:6445–6458

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

We thank J. Boyer, B. Jackson, K. McConnell, and G. Voltaire for assistance in the lab, and two anonymous reviewers for helpful comments on the manuscript. This work was supported by National Institutes of Health grant 1R15GM081862-01A1. This is contribution number 255 of the Louis Calder Center—Biological Field Station, Fordham University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gordon R. Plague.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 63 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Plague, G.R., Dougherty, K.M., Boodram, K.S. et al. Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli . Genetica 139, 895–902 (2011). https://doi.org/10.1007/s10709-011-9593-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10709-011-9593-x

Keywords

Navigation