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Journal of Bacteriology, March 2007, p. 1794-1802, Vol. 189, No. 5
0021-9193/07/$08.00+0     doi:10.1128/JB.00899-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Weak Rolling Adhesion Enhances Bacterial Surface Colonization{triangledown} ,{dagger}

Brett N. Anderson,1 Albert M. Ding,1 Lina M. Nilsson,2 Kaoru Kusuma,1 Veronika Tchesnokova,3 Viola Vogel,2 Evgeni V. Sokurenko,3 and Wendy E. Thomas1*

Department of Bioengineering, University of Washington, Seattle, Washington,1 Laboratory for Biologically Oriented Materials, Department of Materials, ETH Zurich, Zürich, Switzerland,2 Department of Microbiology, University of Washington, Seattle, Washington3

Received 22 June 2006/ Accepted 8 December 2006

Bacterial adhesion to and subsequent colonization of surfaces are the first steps toward forming biofilms, which are a major concern for implanted medical devices and in many diseases. It has generally been assumed that strong irreversible adhesion is a necessary step for biofilm formation. However, some bacteria, such as Escherichia coli when binding to mannosylated surfaces via the adhesive protein FimH, adhere weakly in a mode that allows them to roll across the surface. Since single-point mutations or even increased shear stress can switch this FimH-mediated adhesion to a strong stationary mode, the FimH system offers a unique opportunity to investigate the role of the strength of adhesion independently from the many other factors that may affect surface colonization. Here we compare levels of surface colonization by E. coli strains that differ in the strength of adhesion as a result of flow conditions or point mutations in FimH. We show that the weak rolling mode of surface adhesion can allow a more rapid spreading during growth on a surface in the presence of fluid flow. Indeed, an attempt to inhibit the adhesion of strongly adherent bacteria by blocking mannose receptors with a soluble inhibitor actually increased the rate of surface colonization by allowing the bacteria to roll. This work suggests that (i) a physiological advantage to the weak adhesion demonstrated by commensal variants of FimH bacteria may be to allow rapid surface colonization and (ii) antiadhesive therapies intended to prevent biofilm formation can have the unintended effect of enhancing the rate of surface colonization.

* Corresponding author. Mailing address: Department of Bioengineering, University of Washington, 1705 NE Pacific St., Foege N430P (Box 355061), Seattle, WA 98195-5061. Phone: (206) 616-3947. Fax: (206) 685-3300. E-mail: wendyt{at}u.washington.edu.

{triangledown} Published ahead of print on 22 December 2006.

{dagger} Supplemental material for this article may be found at http://jb.asm.org/.

Journal of Bacteriology, March 2007, p. 1794-1802, Vol. 189, No. 5
0021-9193/07/$08.00+0     doi:10.1128/JB.00899-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Ronald, L. S., Yakovenko, O., Yazvenko, N., Chattopadhyay, S., Aprikian, P., Thomas, W. E., Sokurenko, E. V. (2008). From the Cover: Adaptive mutations in the signal peptide of the type 1 fimbrial adhesin of uropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA 105: 10937-10942 [Abstract] [Full Text]  
  • Yakovenko, O., Sharma, S., Forero, M., Tchesnokova, V., Aprikian, P., Kidd, B., Mach, A., Vogel, V., Sokurenko, E., Thomas, W. E. (2008). FimH Forms Catch Bonds That Are Enhanced by Mechanical Force Due to Allosteric Regulation. J. Biol. Chem. 283: 11596-11605 [Abstract] [Full Text]  
  • Weissman, S. J., Beskhlebnaya, V., Chesnokova, V., Chattopadhyay, S., Stamm, W. E., Hooton, T. M., Sokurenko, E. V. (2007). Differential Stability and Trade-Off Effects of Pathoadaptive Mutations in the Escherichia coli FimH Adhesin. Infect. Immun. 75: 3548-3555 [Abstract] [Full Text]  


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