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Pilus retraction powers bacterial twitching motility

Naturevolume 407, pages98–102 (2000)Cite this article

Abstract

Twitching and social gliding motility allow many Gram negative bacteria to crawl along surfaces, and are implicated in a wide range of biological functions1. Type IV pili (Tfp) are required for twitching and social gliding, but the mechanism by which these filaments promote motility has remained enigmatic1,2,3,4. Here we use laser tweezers5 to show that Tfp forcefully retract.Neisseria gonorrhoeae cells that produce Tfp actively crawl on a glass surface and form adherent microcolonies. When laser tweezers are used to place and hold cells near a microcolony, retractile forces pull the cells toward the microcolony. In quantitative experiments, the Tfp of immobilized bacteria bind to latex beads and retract, pulling beads from the tweezers at forces that can exceed 80 pN. Episodes of retraction terminate with release or breakage of the Tfp tether. Both motility and retraction mediated by Tfp occur at about 1 µm s-1 and require protein synthesis and function of the PilT protein. Our experiments establish that Tfp filaments retract, generate substantial force and directly mediate cell movement.

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Figure 1: PiliatedN. gonorrhoeae cells crawl on an inert surface.
Figure 2: Optical tweezers reveal retractile forces between piliatedN. gonorrhoeae cells.
Figure 3: Quantitative type IV pili retraction assay.

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References

  1. Wall, D. & Kaiser, D. Type IV pili and cell motility. Mol. Microbiol.32, 1–10 (1999).

    Article CAS PubMed  Google Scholar 

  2. Henrichsen, J. Twitching motility.Annu. Rev. Microbiol.37, 81–93 (1983).

    Article CAS PubMed  Google Scholar 

  3. Bradley, D. E. A function ofPseudomonas aeruginosa PAO polar pili: twitching motility.Can. J. Microbiol.26, 146– 154 (1980).

    Article CAS PubMed  Google Scholar 

  4. Wolfgang, M., Park, H. S., Hayes, S. F., van Putten, J. P. M. & Koomey, M. Suppression of an absolute defect in type IV pilus biogenesis by loss-of-function mutations inpilT, a twitching motility gene inNeisseria gonorrhoeae.Proc. Natl Acad. Sci. USA95, 14973– 14978 (1998).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  5. Sheetz, M. P. (ed.) Laser Tweezers in Cell Biology (Academic, New York, 1997).

    Google Scholar 

  6. Swanson, J. Studies on gonococcus infection. XII. Colony color and opacity variants of gonococci.Infect. Immun.19, 320– 331 (1978).

    CAS PubMed PubMed Central  Google Scholar 

  7. O'Toole, G. A. & Kolter, R. Flagellar and twitching motility are necessary forPseudomonas aeruginosa biofilm development. Mol. Microbiol.30, 295–304 (1998).

    Article CAS PubMed  Google Scholar 

  8. Bieber, D.et al. Type IV pili, transient bacterial aggregates, and virulence of enteropathogenicEscherichia coli.Science280, 2114–2118 (1998).

    Article ADS CAS PubMed  Google Scholar 

  9. Comolli, J. C. et al.Pseudomonas aeruginosa gene products PilT and PilU are required for cytotoxicity in vitro and virulence in a mouse model of acute pneumonia.Infect. Immun.67, 3625– 3630 (1999).

    CAS PubMed PubMed Central  Google Scholar 

  10. Pujol, C., Eugene, E., Marceau, M. & Nassif, X. The meningococcal PilT protein is required for induction of intimate attachment to epithelial cells following pilus-mediated adhesion.Proc. Natl Acad. Sci. USA96, 4017–4022 ( 1999).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  11. Merz, A. J., Enns, C. A. & So, M. Type IV pili of pathogenicNeisseriae elicit cortical plaque formation in epithelial cells.Mol. Microbiol.32, 1316–1332 (1999).

    Article CAS PubMed  Google Scholar 

  12. Seifert, H. S., Ajioka, R. S., Marchal, C., Sparling, P. F. & So, M. DNA transformation leads to pilin antigenic variation inNeisseria gonorrhoeae.Nature336, 392–395 (1988).

    Article ADS CAS PubMed  Google Scholar 

  13. Dubnau, D. DNA uptake in bacteria.Annu. Rev. Microbiol.53, 217–244 (1999).

    Article CAS PubMed  Google Scholar 

  14. Yoshida, T., Kim, S. R. & Komano, T. Twelvepil genes are required for biogenesis of the R64 thin pilus.J. Bacteriol.181, 2038–2043 (1999).

    CAS PubMed PubMed Central  Google Scholar 

  15. Bradley, D. E. Evidence for the retraction ofPseudomonas aeruginosa RNA phage pili.Biochem. Biophys. Res. Commun.47, 142– 149 (1972).

    Article CAS PubMed  Google Scholar 

  16. Karaolis, D. K., Somara, S., Maneval, D. R. Jr, Johnson, J. A. & Kaper, J. B. A bacteriophage encoding a pathogenicity island, a type-IV pilus and a phage receptor in cholera bacteria.Nature399, 375– 379 (1999).

    Article ADS CAS PubMed  Google Scholar 

  17. Parge, H. E. et al. Structure of the fibre-forming protein pilin at 2.6 Å resolution.Nature378, 32– 38 (1995).

    ADS CAS PubMed  Google Scholar 

  18. Forest, K. T. & Tainer, J. A. Type-4 pilus structure: outside to inside and top to bottom—a minireview.Gene 192, 165–169 (1997).

    Article CAS PubMed  Google Scholar 

  19. Whitchurch, C. B., Hobbs, M., Livingston, S. P., Krishnapillai, V. & Mattick, J. S. Characterisation of aPseudomonas aeruginosa twitching motility gene and evidence for a specialised protein export system widespread in eubacteria.Gene101, 33–44 (1991).

    Article CAS PubMed  Google Scholar 

  20. Wolfgang, M. et al.pilT mutations lead to simultaneous defects in competence for natural transformation and twitching motility in piliatedNeisseria gonorrhoeae.Mol. Microbiol.29, 321 –330 (1998).

    Article CAS PubMed  Google Scholar 

  21. Brossay, L., Paradis, G., Fox, R., Koomey, M. & Hebert, J. Identification, localization, and distribution of the PilT protein inNeisseria gonorrhoeae.Infect. Immun. 62, 2302–2308 (1994).

    CAS PubMed PubMed Central  Google Scholar 

  22. Krause, S. et al. Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by thecag pathogenicity island ofHelicobacter pylori share similar hexameric ring structures.Proc. Natl Acad. Sci. USA97, 3067–3072 (2000).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  23. Novotny, C. P. & Fives-Taylor, P. Retraction of F pili.J. Bacteriol.117, 1306– 1311 (1974).

    CAS PubMed PubMed Central  Google Scholar 

  24. Ginocchio, C. C., Olmsted, S. B., Wells, C. L. & Galan, J. E. Contact with epithelial cells induces the formation of surface appendages onSalmonella typhimurium.Cell76, 717–724 (1994).

    Article CAS PubMed  Google Scholar 

  25. Evans, E., Berk, D. & Leung, A. Detachment of agglutinin-bonded red blood cells. I. Forces to rupture molecular-point attachments.Biophys. J.59, 838– 848 (1991).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  26. Shao, J. Y., Ting-Beall, H. P. & Hochmuth, R. M. Static and dynamic lengths of neutrophil microvilli.Proc. Natl Acad. Sci. USA95, 6797– 6802 (1998).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  27. Coppin, C. M., Finer, J. T., Spudich, J. A. & Vale, R. D. Detection of sub-8-nm movements of kinesin by high-resolution optical-trap microscopy.Proc. Natl Acad. Sci. USA93, 1913–1917 (1996).

    Article ADS CAS PubMed PubMed Central  Google Scholar 

  28. Mahadevan, L. & Matsudaira, P. Motility powered by supramolecular springs and ratchets.Science288, 95– 100 (2000).

    Article ADS CAS PubMed  Google Scholar 

  29. Dupuy, B., Taha, M. K., Pugsley, A. P. & Marchal, C. Neisseria gonorrhoeae prepilin export studied inEscherichia coli.J. Bacteriol.173, 7589– 7598 (1991).

    Article CAS PubMed PubMed Central  Google Scholar 

  30. Felsenfeld, D. P., Schwartzberg, P. L., Venegas, A., Tse, R. & Sheetz, M. P. Selective regulation of integrin-cytoskeleton interactions by the tyrosine kinase Src.Nature Cell Biol. 1, 200–206 (1999).

    Article CAS PubMed  Google Scholar 

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Acknowledgements

We thank our colleagues in the Sheetz and So labs for invaluable technical assistance and stimulating discussions; E. Barklis and L. Kenney for critical comments on the manuscript; and M. Koomey for providing bacterial strains. This work was supported by NIH grants to M.S. and M.P.S. A.J.M. received pre-doctoral support from an NIH NRSA grant and postdoctoral support from the Cancer Research Fund of the Damon Runyan-Walter Winchell Foundation.

Author information

Author notes

  1. Alexey J. Merz

    Present address: Department of Biochemistry, Dartmouth Medical School, Hanover, New Hampshire, 03755-3844, USA

  2. Michael P. Sheetz

    Present address: Department of Biological Sciences, Columbia University, New York, New York, 10027, USA

Authors and Affiliations

  1. Department of Molecular Microbiology and Immunology, Oregon Health Sciences University, Portland, 97201-3098, Oregon, USA

    Alexey J. Merz & Magdalene So

  2. Department of Cell Biology, Duke University Medical School, Durham, 27705, North Carolina, USA

    Michael P. Sheetz

Authors
  1. Alexey J. Merz
  2. Magdalene So
  3. Michael P. Sheetz

Corresponding author

Correspondence toMichael P. Sheetz.

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Merz, A., So, M. & Sheetz, M. Pilus retraction powers bacterial twitching motility.Nature407, 98–102 (2000). https://doi.org/10.1038/35024105

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