1887

Abstract

Aggregation of microbial cells mediated by specific interactions plays a pivotal role in the natural environment, in medicine and in biotechnological processes. Here we used atomic force microscopy (AFM) to measure individual lectin–carbohydrate interactions involved in the flocculation of yeast cells, an aggregation event of crucial importance in fermentation technology. AFM probes functionalized with oligoglucose carbohydrates were used to record force-distance curves on living yeast cells at a rate of 0·5 μm s. Flocculating cells showed adhesion forces of 121±53 pN, reflecting the specific interaction between individual cell-surface lectins and glucose residues. Similar adhesion forces, 117±41 pN, were measured using probes functionalized with the lectin concanavalin A and attributed to specific binding to cell-surface mannose residues. By contrast, specific interaction forces were not observed in non-flocculating conditions, i.e. in the presence of mannose or when using non-flocculating cells, pointing to their involvement in yeast flocculation. The single molecule force spectroscopy measurements presented here provide a means to study a variety of cellular interactions at the molecular level, such as the adhesion of bacteria to animal and plant tissues.

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2003-10-01
2019-10-14
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References

  1. Abu-Lail, N. I. & Camesano, T. A. ( 2002; ). Elasticity of Pseudomonas putida KT2442 surface polymers probed with single-molecule force microscopy. Langmuir 18, 4071–4081.[CrossRef]
    [Google Scholar]
  2. Ahimou, F., Touhami, A. & Dufrêne, Y. F. ( 2003; ). Real-time imaging of the surface topography of living yeast cells by atomic force microscopy. Yeast 20, 25–30.[CrossRef]
    [Google Scholar]
  3. Benoit, M., Gabriel, D., Gerisch, G. & Gaub, H. E. ( 2000; ). Discrete interactions in cell adhesion measured by single-molecule force spectroscopy. Nature Cell Biol 2, 313–317.[CrossRef]
    [Google Scholar]
  4. Binnig, G., Quate, C. F. & Gerber, C. ( 1986; ). Atomic force microscope. Phys Rev Lett 56, 930–933.[CrossRef]
    [Google Scholar]
  5. Bowen, W. R., Lovitt, R. W. & Wright, C. J. ( 2000; ). Direct quantification of Aspergillus niger spore adhesion in liquid using an atomic force microscope. J Colloid Interf Sci 228, 428–433.[CrossRef]
    [Google Scholar]
  6. Busscher, H. J. & van der Mei, H. C. ( 1995; ). Use of flow chamber devices and image analysis methods to study microbial cell adhesion. Methods Enzymol 253, 455–477.
    [Google Scholar]
  7. Busscher, H. J., Handley, P. S., Bos, R. & van der Mei, H. C. ( 1999; ). Physico-chemistry of microbial adhesion from an overall approach to the limits. In Physical Chemistry of Biological Interfaces, pp. 431–445. Edited by A. Baszkin & W. Norde. New York: Marcel Dekker.
  8. Calleja, G. B. ( 1989; ). Cell Aggregation. In The Yeasts, Vol. 2. Yeast and Environment, pp. 165–238. Edited by A. H. Rose & J. S. Harrison. London: Academic Press.
  9. Camesano, T. A. & Logan, B. E. ( 2000; ). Probing bacterial electrosteric interactions using atomic force microscopy. Environ Sci Technol 34, 3354–3362.[CrossRef]
    [Google Scholar]
  10. Cleveland, J. P., Manne, S., Bocek, D. & Hansma, P. K. ( 1993; ). A nondestructive method for determining the spring constant of cantilevers for scanning force microscopy. Rev Sci Instrum 64, 403–405.[CrossRef]
    [Google Scholar]
  11. Costerton, J. W., Stewart, P. S. & Greenberg, E. P. ( 1999; ). Bacterial biofilms: a common cause of persistent infections. Science 284, 1318–1322.[CrossRef]
    [Google Scholar]
  12. Dammer, U., Hegner, M., Anselmetti, D., Wagner, P., Dreier, M., Huber, W. & Güntherodt, H. J. ( 1996; ). Specific antigen/antibody interactions measured by force microscopy. Biophys J 70, 2437–2441.[CrossRef]
    [Google Scholar]
  13. Dengis, P. B., Nélissen, L. R. & Rouxhet, P. G. ( 1995; ). Mechanisms of yeast flocculation: comparison of top- and bottom-fermenting strains. Appl Environ Microbiol 61, 718–728.
    [Google Scholar]
  14. Dufrêne, Y. F. ( 2002; ). Atomic force microscopy, a powerful tool in microbiology. J Bacteriol 184, 5205–5213.[CrossRef]
    [Google Scholar]
  15. Dufrêne, Y. F. ( 2003; ). Recent progress in the application of atomic force microscopy imaging and force spectroscopy to microbiology. Curr Opin Microbiol 6, 317–323.[CrossRef]
    [Google Scholar]
  16. Dufrêne, Y. F., Boonaert, C. J. P., Gerin, P. A., Asther, M. & Rouxhet, P. G. ( 1999; ). Direct probing of the surface ultrastructure and molecular interaction of dormant and germinating spores of Phanerochaete chrysosporium. J Bacteriol 181, 5350–5354.
    [Google Scholar]
  17. Florin, E.-L., Moy, V. T. & Gaub, H. E. ( 1994; ). Adhesion forces between individual ligand-receptor pairs. Science 264, 415–417.[CrossRef]
    [Google Scholar]
  18. Gad, M., Itoh, A. & Ikai, A. ( 1997; ). Mapping cell wall polysaccharides of living microbial cells using atomic force microscopy. Cell Biol Int 21, 697–706.[CrossRef]
    [Google Scholar]
  19. Hinterdorfer, P., Baumgartner, W., Gruber, H. J., Schilcher, K. & Schindler, H. ( 1996; ). Detection and localization of individual antibody–antigen recognition events by atomic force microscopy. Proc Natl Acad Sci U S A 93, 3477–3481.[CrossRef]
    [Google Scholar]
  20. Jin, Y. L. & Speers, R. A. ( 1998; ). Flocculation of Saccharomyces cerevisiae. Food Res Int 31, 421–440.[CrossRef]
    [Google Scholar]
  21. Johnsson, B., Löfas, S. & Lindquist, G. ( 1991; ). Immobilization of proteins to a carboxymethyldextran-modified gold surface for biospecific interaction analysis in surface plasmon resonance sensors. Anal Biochem 198, 268–277.[CrossRef]
    [Google Scholar]
  22. Lee, G. U., Chrisey, L. A. & Colton, R. J. ( 1994; ). Direct measurement of the forces between complementary strands of DNA. Science 266, 771–773.[CrossRef]
    [Google Scholar]
  23. Lower, S. K., Hochella, M. F. & Beveridge, T. J. ( 2001; ). Bacterial recognition of mineral surfaces: nanoscale interactions between Shewanella and α-FeOOH. Science 292, 1360–1363.[CrossRef]
    [Google Scholar]
  24. Miki, B. L. A., Poon, N. H., James, A. P. & Seligy, V. L. ( 1982; ). Possible mechanism for flocculation interactions governed by gene FLO1 in Saccharomyces cerevisiae. J Bacteriol 150, 878–889.
    [Google Scholar]
  25. Müller, D. J., Baumeister, W. & Engel, A. ( 1999; ). Controlled unzipping of a bacterial surface layer with atomic force microscopy. Proc Natl Acad Sci U S A 96, 13170–13174.[CrossRef]
    [Google Scholar]
  26. Razatos, A., Ong, Y.-L., Sharma, M. M. & Georgiou, G. ( 1998; ). Molecular determinants of bacterial adhesion monitored by atomic force microscopy. Proc Natl Acad Sci U S A 95, 11059–11064.[CrossRef]
    [Google Scholar]
  27. Savage, D. C. & Fletcher, M. (editors) ( 1985; ). Bacterial Adhesion. New York, London: Plenum.
  28. Stratford, M. ( 1992; ). Yeast flocculation: a new perspective. Adv Microbiol Physiol 33, 1–71.
    [Google Scholar]
  29. Touhami, A., Hoffmann, B., Vasella, A., Denis, F. & Dufrêne, Y. F. ( 2003; ). Probing specific lectin-carbohydrate interactions using atomic force microscopy imaging and force measurements. Langmuir 19, 1745–1751.[CrossRef]
    [Google Scholar]
  30. van der Aa, B. C., Michel, R. M., Asther, M., Zamora, M. T., Rouxhet, P. G. & Dufrêne, Y. F. ( 2001; ). Stretching cell surface macromolecules by atomic force microscopy. Langmuir 17, 3116–3119.[CrossRef]
    [Google Scholar]
  31. Watnick, P. & Kolter, R. ( 2000; ). Biofilm, city of microbes. J Bacteriol 182, 2675–2679.[CrossRef]
    [Google Scholar]
  32. Xu, W., Mulhern, P. J., Blackford, B. L., Jericho, M. H., Firtel, M. & Beveridge, T. J. ( 1996; ). Modeling and measuring the elastic properties of an archaeal surface, the sheath of Methanospirillum hungatei, and the implication for methane production. J Bacteriol 178, 3106–3112.
    [Google Scholar]
  33. Yao, X., Jericho, M., Pink, D. & Beveridge, T. ( 1999; ). Thickness and elasticity of gram-negative murein sacculi measured by atomic force microscopy. J Bacteriol 181, 6865–6875.
    [Google Scholar]
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