European Biophysics Journal

, Volume 44, Issue 5, pp 291–300 | Cite as

Rigid multibody simulation of a helix-like structure: the dynamics of bacterial adhesion pili

  • Johan Zakrisson
  • Krister Wiklund
  • Martin Servin
  • Ove Axner
  • Claude Lacoursière
  • Magnus AnderssonEmail author
Original Paper


We present a coarse-grained rigid multibody model of a subunit assembled helix-like polymer, e.g., adhesion pili expressed by bacteria, that is capable of describing the polymer’s force-extension response. With building blocks representing individual subunits, the model appropriately describes the complex behavior of pili expressed by the gram-negative uropathogenic Escherichia coli bacteria under the action of an external force. Numerical simulations show that the dynamics of the model, which include the effects of both unwinding and rewinding, are in good quantitative agreement with the characteristic force-extension response as observed experimentally for type 1 and P pili. By tuning the model, it is also possible to reproduce the force-extension response in the presence of anti-shaft antibodies, which dramatically changes the mechanical properties. Thus, the model and results in this work give enhanced understanding of how a pilus unwinds under the action of external forces and provide a new perspective of the complex bacterial adhesion processes.


Fimbriae Escherichia coli Optical tweezers Simulations Force spectroscopy 



This work was performed within the Umeå Centre for Microbial Research (UCMR) Linnaeus Program supported by Umeå University and the Swedish Research Council (349-2007-8673) and supported by the Swedish Research Council (621-2013-5379) to M.A.

Supplementary material

249_2015_1021_MOESM1_ESM.mpg (1.8 mb)
Supplementary material 1 (MPG 1848 kb)


  1. Andersson M, Fällman E, Uhlin BE, Axner O (2006a) Dynamic force spectroscopy of E. coli P pili. Biophys J 91:2717–2725. doi: 10.1529/biophysj.106.087429 PubMedCentralPubMedCrossRefGoogle Scholar
  2. Andersson M, Fällman E, Uhlin BE, Axner O (2006b) A sticky chain model of the elongation and unfolding of Escherichia coli P pili under stress. Biophys J 90:1521–1534. doi: 10.1529/biophysj.105.074674 PubMedCentralPubMedCrossRefGoogle Scholar
  3. Andersson M, Fällman E, Uhlin BE, Axner O (2006c) Force measuring optical tweezers system for long time measurements of P pili stability. Proc SPIE 6088:286–295. doi: 10.1117/12.642206 Google Scholar
  4. Andersson M, Uhlin BE, Fällman E (2007) The biomechanical properties of E. coli pili for urinary tract attachment reflect the host environment. Biophys J 93:3008–3014. doi: 10.1529/biophysj.107.110643 PubMedCentralPubMedCrossRefGoogle Scholar
  5. Andersson M, Axner O, Almqvist F et al (2008) Physical properties of biopolymers assessed by optical tweezers: analysis of folding and refolding of bacterial pili. ChemPhysChem 9:221–235. doi: 10.1002/cphc.200700389 PubMedCrossRefGoogle Scholar
  6. Andersson M, Björnham O, Svantesson M et al (2012) A structural basis for sustained bacterial adhesion: biomechanical properties of CFA/I pili. J Mol Biol 415:918–928. doi: 10.1016/j.jmb.2011.12.006 PubMedCentralPubMedCrossRefGoogle Scholar
  7. Axner O, Björnham O, Castelain M, et al (2010) Unraveling the secrets of bacterial adhesion organelles using single molecule force spectroscopy. In: Gräslund A, Rigler R, Widengren J (eds) single molecule spectroscopy in Chemistry, Physics and Biology, Springer Ser. Chem Phys. Springer, Berlin, pp 337–362Google Scholar
  8. Björnham O, Axner O, Andersson M (2008) Modeling of the elongation and retraction of Escherichia coli P pili under strain by Monte Carlo simulations. Eur Biophys J 37:381–391. doi: 10.1007/s00249-007-0223-6 PubMedCrossRefGoogle Scholar
  9. Bullitt E, Makowski L (1998) Bacterial adhesion pili are heterologous assemblies of similar subunits. Biophys J 74:623–632. doi: 10.1016/S0006-3495(98)77821-X PubMedCentralPubMedCrossRefGoogle Scholar
  10. Castelain M, Koutris E, Andersson M et al (2009) Characterization of the biomechanical properties of T4 pili expressed by Streptococcus pneumoniae—a comparison between helix-like and open coil-like pili. ChemPhysChem 10:1533–1540. doi: 10.1002/cphc.200900195 PubMedCrossRefGoogle Scholar
  11. Castelain M, Ehlers S, Klinth JE et al (2011) Fast uncoiling kinetics of F1C pili expressed by uropathogenic Escherichia coli are revealed on a single pilus level using force-measuring optical tweezers. Eur Biophys J 40:305–316. doi: 10.1007/s00249-010-0648-1 PubMedCrossRefGoogle Scholar
  12. Duncan MJ, Mann EL, Cohen MS et al (2005) The distinct binding specificities exhibited by enterobacterial type 1 fimbriae are determined by their fimbrial shafts. J Biol Chem 280:37707–37716. doi: 10.1074/jbc.M501249200 PubMedCrossRefGoogle Scholar
  13. Fällman E, Schedin S, Jass J et al (2004) Optical tweezers based force measurement system for quantitating binding interactions: system design and application for the study of bacterial adhesion. Biosens Bioelectron 19:1429–1437. doi: 10.1016/j.bios.2003.12.029 PubMedCrossRefGoogle Scholar
  14. Fällman E, Schedin S, Jass J et al (2005) The unfolding of the P pili quaternary structure by stretching is reversible, not plastic. EMBO Rep 6:52–56. doi: 10.1038/sj.embor.7400310 PubMedCentralPubMedCrossRefGoogle Scholar
  15. Forero M, Yakovenko O, Sokurenko EV et al (2006) Uncoiling mechanics of Escherichia coli type I fimbriae are optimized for catch bonds. PLoS Biol 4:1509–1516. doi: 10.1371/journal.pbio.0040298 CrossRefGoogle Scholar
  16. Hahn E, Wild P, Hermanns U et al (2002) Exploring the 3D molecular architecture of Escherichia coli type 1 Pili. J Mol Biol 323:845–857. doi: 10.1016/S0022-2836(02)01005-7 PubMedCrossRefGoogle Scholar
  17. Klinth JE, Pinkner JS, Hultgren SJ et al (2012) Impairment of the biomechanical compliance of P pili: a novel means of inhibiting uropathogenic bacterial infections? Eur Biophys J 41:285–295. doi: 10.1007/s00249-011-0784-2 PubMedCentralPubMedCrossRefGoogle Scholar
  18. Lacoursière C (2007) Ghosts and machines: regularized variational Methods for interactive simulations of multibodies with dry frictional contacts, PhD thesis, Umeå UniversityGoogle Scholar
  19. Li Y-F, Poole S, Nishio K et al (2009) Structure of CFA/I fimbriae from enterotoxigenic Escherichia coli. Proc Natl Acad Sci USA 106:10793–10798. doi: 10.1073/pnas.0812843106 PubMedCentralPubMedCrossRefGoogle Scholar
  20. Lugmaier Ra, Schedin S, Kühner F, Benoit M (2008) Dynamic restacking of Escherichia coli P-pili. Eur Biophys J 37:111–120. doi: 10.1007/s00249-007-0183-x PubMedCrossRefGoogle Scholar
  21. Miller E, Garcia T, Hultgren SJ, Oberhauser AF (2006) The mechanical properties of E. coli type 1 pili measured by atomic force microscopy techniques. Biophys J 91:3848–3856. doi: 10.1529/biophysj.106.088989 PubMedCentralPubMedCrossRefGoogle Scholar
  22. Mortezaei N, Singh B, Bullitt E et al (2013) P-fimbriae in the presence of anti-PapA antibodies: new insight of antibodies action against pathogens. Sci Rep 3:3393. doi: 10.1038/srep03393 PubMedCentralPubMedCrossRefGoogle Scholar
  23. Mortezaei N, Epler CR, S PP et al (2015) Structure and function of Enterotoxigenic Escherichia coli fimbriae from differing assembly pathways. Mol Microbiol 95:116–126. doi: 10.1111/mmi.12847 PubMedCrossRefGoogle Scholar
  24. Mu X-Q, Bullitt E (2006) Structure and assembly of P-pili: a protruding hinge region used for assembly of a bacterial adhesion filament. Proc Natl Acad Sci USA 103:9861–9866. doi: 10.1073/pnas.0509620103 PubMedCentralPubMedCrossRefGoogle Scholar
  25. Rangel DE, Marín-Medina N, Castro JE et al (2013) Observation of bacterial type I pili extension and contraction under fluid flow. PLoS one 8:e65563. doi: 10.1371/journal.pone.0065563 PubMedCentralPubMedCrossRefGoogle Scholar
  26. Sauer F, Mulvey M, Schilling J et al (2000) Bacterial pili: molecular mechanisms of pathogenesis. Curr Opin microbiol 3:65–72PubMedCrossRefGoogle Scholar
  27. Schwan WR, Lee JL, Lenard FA et al (2002) Osmolarity and pH growth conditions regulate fim gene transcription and type 1 pilus expression in uropathogenic Escherichia coli. Infect Immun 70:1391. doi: 10.1128/IAI.70.3.1391 PubMedCentralPubMedCrossRefGoogle Scholar
  28. Servin M, Lacoursière C (2007) Rigid body cable for virtual environments. IEEE Trans Vis Comput Graph 14:783–796. doi: 10.1109/TVCG.2007.70629 CrossRefGoogle Scholar
  29. Verger D, Bullitt E, Hultgren SJ, Waksman G (2007) Crystal structure of the P pilus rod subunit PapA. PLoS Pathog 3:e73. doi: 10.1371/journal.ppat.0030073 PubMedCentralPubMedCrossRefGoogle Scholar
  30. Zakrisson J, Wiklund K, Axner O, Andersson M (2012) Helix-like biopolymers can act as dampers of force for bacteria in flows. Eur Biophys J 41:551–560. doi: 10.1007/s00249-012-0814-8 PubMedCrossRefGoogle Scholar
  31. Zakrisson J, Wiklund K, Axner O, Andersson M (2013) The shaft of the type 1 fimbriae regulates an externalforce to match the FimH catch bond. Biophys J 104:2137–2148. doi: 10.1016/j.bpj.2013.03.059 PubMedCentralPubMedCrossRefGoogle Scholar

Copyright information

© European Biophysical Societies' Association 2015

Authors and Affiliations

  • Johan Zakrisson
    • 1
  • Krister Wiklund
    • 1
  • Martin Servin
    • 1
  • Ove Axner
    • 1
    • 3
  • Claude Lacoursière
    • 2
  • Magnus Andersson
    • 1
    • 3
    Email author
  1. 1.Department of PhysicsUmeå UniversityUmeåSweden
  2. 2.Department of Computer ScienceUmeå UniversityUmeåSweden
  3. 3.Umeå Centre for Microbial Research (UCMR)Umeå UniversityUmeåSweden

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