Journal of Molecular Evolution

, Volume 84, Issue 5–6, pp 279–284 | Cite as

Transposable Elements Mediate Adaptive Debilitation of Flagella in Experimental Escherichia coli Populations

  • Gordon R. Plague
  • Krystal S. Boodram
  • Kevin M. Dougherty
  • Sandar Bregg
  • Daniel P. Gilbert
  • Hira Bakshi
  • Daniel Costa
Original Article

Abstract

Although insertion sequence (IS) elements are generally considered genomic parasites, they can mediate adaptive genetic changes in bacterial genomes. We discovered that among 12 laboratory-evolved Escherichia coli populations, three had experienced at least six different IS1-mediated deletions of flagellar genes. These deletions all involved the master flagellar regulator flhDC, and as such completely incapacitate motility. Two lines of evidence strongly suggest that these deletions were adaptive in our evolution experiment: (1) parallel evolution in three independent populations is highly unlikely just by chance, and (2) one of these deletion mutations swept to fixation within ~1000 generations, which is over two million times faster than expected if this deletion was instead selectively neutral and thus evolving by genetic drift. Because flagella are energetically expensive to synthesize and operate, we suspect that debilitating their construction conferred a fitness advantage in our well-stirred evolution experiment. These findings underscore the important role that IS elements can play in mediating adaptive loss-of-function mutations in bacteria.

Keywords

Adaptive evolution Parallel evolution Natural selection Insertion sequence element Loss-of-function mutation Experimental evolution 

Notes

Acknowledgements

We thank Deea Das for help on this project, and two anonymous reviewers for critically reviewing the manuscript. This work was supported by grant R15GM081862 from the National Institutes of Health.

References

  1. Andersson SGE, Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6:263–268CrossRefPubMedGoogle Scholar
  2. Barker CS, Prüß BM, Matsumura P (2004) Increased motility of Escherichia coli by insertion sequence element integration into the regulatory region of the flhD operon. J Bacteriol 186:7529–7537CrossRefPubMedPubMedCentralGoogle Scholar
  3. Blattner FR et al (1997) The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462CrossRefPubMedGoogle Scholar
  4. Casacuberta E, González J (2013) The impact of transposable elements in environmental adaptation. Mol Ecol 22:1503–1517CrossRefPubMedGoogle Scholar
  5. 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, DC, pp 305–366CrossRefGoogle Scholar
  6. Chou HH, Marx CJ (2012) Optimization of gene expression through divergent mutational paths. Cell Rep 1:133–140CrossRefPubMedPubMedCentralGoogle Scholar
  7. Chou HH, Berthet J, Marx CJ (2009) Fast growth increases the selective advantage of a mutation arising recurrently during evolution under metal limitation. PLoS Genet 5:e1000652CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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 183:2834–2841CrossRefPubMedPubMedCentralGoogle Scholar
  9. de Visser JAGM, Akkermans ADL, Hoekstra RF, de Vos WM (2004) Insertion-sequence-mediated mutations isolated during adaptation to growth and starvation in Lactococcus lactis. Genetics 168:1145–1157CrossRefPubMedPubMedCentralGoogle Scholar
  10. Doolittle WF, Sapienza C (1980) Selfish genes, the phenotype paradigm and genome evolution. Nature 284:601–603CrossRefPubMedGoogle Scholar
  11. Edwards RJ, Sockett RE, Brookfield JFY (2002) A simple method for genome-wide screening for advantageous insertions of mobile DNAs in Escherichia coli. Curr Biol 12:863–867CrossRefPubMedGoogle Scholar
  12. Gaffé J, McKenzie C, Maharjan RP, Coursange E, Ferenci T, Schneider D (2011) Insertion sequence-driven evolution of Escherichia coli in chemostats. J Mol Evol 72:398–412CrossRefPubMedGoogle Scholar
  13. Hartl DL, Clark AG (1997) Principles of population genetics, 3rd edn. Sinauer Associates, SunderlandGoogle Scholar
  14. He S, Hickman AB, Varani AM, Siguier P, Chandler M, Dekker JP, Dyda F (2015) Insertion sequence IS26 reorganizes plasmids in clinically isolated multidrug-resistant bacteria by replicative transposition. mBio 6:e00715–e00762Google Scholar
  15. Hottes AK, Freddolino PL, Khare A, Donnell ZN, Liu JC, Tavazoie S (2013) Bacterial adaptation through loss of function. PLoS Genet 9:e1003617CrossRefPubMedPubMedCentralGoogle Scholar
  16. Kang Y, Durfee T, Glasner JD, Qiu Y, Frisch D, Winterberg KM, Blattner FR (2004) Systematic mutagenesis of the Escherichia coli genome. J Bacteriol 186:4921–4930CrossRefPubMedPubMedCentralGoogle Scholar
  17. Keseler IM et al (2013) EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:D605–D612CrossRefPubMedGoogle Scholar
  18. Kimura M, Ohta T (1969) The average number of generations until fixation of a mutant gene in a finite population. Genetics 61:763–771PubMedPubMedCentralGoogle Scholar
  19. Kutsukake K, Ohya Y, Iino T (1990) Transcriptional analysis of the flagellar regulon of Salmonella typhimurium. J Bacteriol 172:741–747CrossRefPubMedPubMedCentralGoogle Scholar
  20. Lee H, Popodi E, Tang H, Foster PL (2012) Rate and molecular spectrum of spontaneous mutations in the bacterium Escherichia coli as determined by whole-genome sequencing. Proc Natl Acad Sci USA 109:E2774–E2783CrossRefPubMedPubMedCentralGoogle Scholar
  21. Liu R, Ochman H (2007) Stepwise formation of the bacterial flagellar system. Proc Natl Acad Sci USA 104:7116–7121CrossRefPubMedPubMedCentralGoogle Scholar
  22. Macnab RM (1996) Flagella and motility. In: Neidhardt FC et al (eds) Escherichia coli and Salmonella: cellular and molecular biology, 2nd edn. ASM Press, Washington, DC, pp 123–145Google Scholar
  23. Neidhardt FC, Bloch PL, Smith DF (1974) Culture medium for enterobacteria. J Bacteriol 119:736–747PubMedPubMedCentralGoogle Scholar
  24. Orgel LE, Crick FHC (1980) Selfish DNA: the ultimate parasite. Nature 284:604–607CrossRefPubMedGoogle Scholar
  25. Parkhill J et al (2001) Genome sequence of Yersinia pestis, the causative agent of plague. Nature 413:523–527CrossRefPubMedGoogle Scholar
  26. Parkhill J et al (2003) Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica. Nat Genet 35:32–40CrossRefPubMedGoogle Scholar
  27. Philippe N, Pelosi L, Lenski RE, Schneider D (2009) Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli. J Bacteriol 191:909–921CrossRefPubMedGoogle Scholar
  28. Plague GR (2010) Intergenic transposable elements are not randomly distributed in Bacteria. Genome Biol Evol 2:584–590CrossRefPubMedPubMedCentralGoogle Scholar
  29. Plague GR, Dougherty KM, Boodram KS, Boustani SE, Cao H, Manning SR, McNally CC (2011) Relaxed natural selection alone does not permit transposable element expansion within 4,000 generations in Escherichia coli. Genetica 139:895–902CrossRefPubMedPubMedCentralGoogle Scholar
  30. Raeside C et al (2014) Large chromosomal rearrangements during a long-term evolution experiment with Escherichia coli. mBio 5:e01314–e01377CrossRefGoogle Scholar
  31. Shapiro JA (1979) Molecular model for the transposition and replication of bacteriophage Mu and other transposable elements. Proc Natl Acad Sci USA 76:1933–1937CrossRefPubMedPubMedCentralGoogle Scholar
  32. Siguier P, Gourbeyre E, Chandler M (2014) Bacterial insertion sequences: their genomic impact and diversity. FEMS Microbiol Rev 38:865–891CrossRefPubMedGoogle Scholar
  33. Song H, Hwang J, Yi H, Ulrich RL, Yu Y, Nierman WC, Kim HS (2010) The early stage of bacterial genome-reductive evolution in the host. PLoS Pathog 6:e1000922CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sousa A, Bourgard C, Wahl LM, Gordo I (2013) Rates of transposition in Escherichia coli. Biol Lett 9:20130838CrossRefPubMedPubMedCentralGoogle Scholar
  35. Soutourina O, Kolb A, Krin E, Laurent-Winter C, Rimsky S, Danchin A, Bertin P (1999) Multiple control of flagellum biosynthesis in Escherichia coli: role of H-NS protein and the cyclic AMP-catabolite activator protein complex in transcription of the flhDC master operon. J Bacteriol 181:7500–7508PubMedPubMedCentralGoogle Scholar
  36. Stern DL (2013) The genetic causes of convergent evolution. Nat Rev Genet 14:751–764CrossRefPubMedGoogle Scholar
  37. Stoebel DM, Hokamp K, Last MS, Dorman CJ (2009) Compensatory evolution of gene regulation in response to stress by Escherichia coli lacking RpoS. PLoS Genet 5:e1000671CrossRefPubMedPubMedCentralGoogle Scholar
  38. Treves DS, Manning S, Adams J (1998) Repeated evolution of an acetate-crossfeeding polymorphism in long-term populations of Escherichia coli. Mol Biol Evol 15:789–797CrossRefPubMedGoogle Scholar
  39. Turlan C, Chandler M (1995) IS1-mediated intramolecular rearrangements: formation of excised transposon circles and replicative deletions. EMBO J 14:5410–5421PubMedPubMedCentralGoogle Scholar
  40. Wagner A (2006) Periodic extinctions of transposable elements in bacterial lineages: evidence from intragenomic variation in multiple genomes. Mol Biol Evol 23:723–733CrossRefPubMedGoogle Scholar
  41. Zhong S, Khodursky A, Dykhuizen DE, Dean AM (2004) Evolutionary genomics of ecological specialization. Proc Natl Acad Sci USA 101:11719–11724CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2017

Authors and Affiliations

  • Gordon R. Plague
    • 1
  • Krystal S. Boodram
    • 2
  • Kevin M. Dougherty
    • 3
  • Sandar Bregg
    • 1
    • 4
  • Daniel P. Gilbert
    • 1
    • 5
  • Hira Bakshi
    • 1
  • Daniel Costa
    • 1
    • 6
  1. 1.Department of BiologyState University of New York at PotsdamPotsdamUSA
  2. 2.Simon Gratz High SchoolPhiladelphiaUSA
  3. 3.Kellogg Biological StationMichigan State UniversityHickory CornersUSA
  4. 4.Department of Environmental Health Sciences, School of Public HealthUniversity of MichiganAnn ArborUSA
  5. 5.School of Engineering LabClarkson UniversityPotsdamUSA
  6. 6.Department of Cell BiologyDuke University Medical CenterDurhamUSA

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