1887

Abstract

This study used atomic force microscopy (AFM) to probe the local cell-surface interactions associated with the glucan polymers of , the macromolecules most commonly attributed to the virulence of this microbe. force spectroscopy was used to quantitatively probe and correlate cell-surface adhesion and dynamics with UA140 wild-type and five glucosyltransferase mutants. Adhesion between the tooth surface and is largely mediated by glucan production from sucrose via three glucosyltransferases (Gtfs; GtfB, GtfC and GtfD). To monitor the contribution of these particular Gtfs, isogenic mutants of were constructed by specific gene inactivation and compared to the wild-type under sucrose and non-sucrose conditions. We report direct measurement of the mechanical properties associated with glucan macromolecules demonstrating that the local adhesion strength increases in a time-dependent process, with a decrease in the average number of rupture events. This finding suggests that attaches mainly through glucans to surfaces in the presence of sucrose. In addition, a possible role of the Gtf proteins in sucrose-independent attachment is supported by the decreased adhesion properties of the GtfBCD mutant compared to the wild-type.

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2007-09-01
2019-10-19
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References

  1. Banas, J. A. & Vickerman, M. M. ( 2003; ). Glucan-binding proteins of the oral streptococci. Crit Rev Oral Biol Med 14, 89–99.[CrossRef]
    [Google Scholar]
  2. Binnig, G., Quate, C. F. & Gerber, C. ( 1986; ). Atomic force microscope. Phys Rev Lett 56, 930–933.[CrossRef]
    [Google Scholar]
  3. Bowen, W. H., Schilling, K., Giertsen, E., Pearson, S., Lee, S. F., Bleiweis, A. & Beeman, D. ( 1991; ). Role of a cell surface-associated protein in adherence and dental caries. Infect Immun 59, 4606–4609.
    [Google Scholar]
  4. Cerning, J. ( 1990; ). Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiol Rev 7, 113–130.
    [Google Scholar]
  5. Costerton, J. W., Lewandowski, Z., Caldwell, D. E., Korber, D. R. & Lappin-Scott, H. M. ( 1995; ). Microbial biofilms. Annu Rev Microbiol 49, 711–745.[CrossRef]
    [Google Scholar]
  6. 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]
  7. Cross, S. E., Kreth, J., Zhu, L., Qi, F. X., Pelling, A. E., Shi, W. Y. & Gimzewski, J. K. ( 2006; ). Atomic force microscopy study of the structure-function relationships of the biofilm-forming bacterium Streptococcus mutans. Nanotechnology 17, S1–S7.[CrossRef]
    [Google Scholar]
  8. Fisher, T. E., Marszalek, P. E. & Fernandez, J. M. ( 2000; ). Stretching single molecules into novel conformations using the atomic force microscope. Nat Struct Biol 7, 719–724.[CrossRef]
    [Google Scholar]
  9. Fukushima, K., Ikeda, T. & Kuramitsu, H. K. ( 1992; ). Expression of Streptococcus mutans gtf genes in Streptococcus milleri. Infect Immun 60, 2815–2822.
    [Google Scholar]
  10. Ghuysen, J. M. & Hackenbeck, R. ( 1994; ). Bacterial Cell Wall. Amsterdam: Elsevier.
  11. Hamada, S. & Slade, H. D. ( 1980; ). Biology, immunology, and cariogenicity of Streptococcus mutans. Microbiol Rev 44, 331–384.
    [Google Scholar]
  12. Kasas, S. & Ikai, A. ( 1995; ). A method for anchoring round shaped cells for atomic force microscope imaging. Biophys J 68, 1678–1680.[CrossRef]
    [Google Scholar]
  13. Kreth, J., Hagerman, E., Tam, K., Merritt, J., Wong, D. T., Wu, B. M., Myung, N. V., Shi, W. & Qi, F. ( 2004; ). Quantitative analyses of Streptococcus mutans biofilms with quartz crystal microbalance, microjet impingement and confocal microscopy. Biofilms 1, 277–284.[CrossRef]
    [Google Scholar]
  14. Kreth, J., Merritt, J., Shi, W. & Qi, F. ( 2005; ). Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol Microbiol 57, 392–404.[CrossRef]
    [Google Scholar]
  15. Kuramitsu, H. K. ( 1993; ). Virulence factors of mutans streptococci: role of molecular genetics. Crit Rev Oral Biol Med 4, 159–176.
    [Google Scholar]
  16. Loesche, W. J. ( 1986; ). Role of Streptococcus mutans in human dental decay. Microbiol Rev 50, 353–380.
    [Google Scholar]
  17. Matsumoto, M., Fujita, K. & Ooshima, T. ( 2006; ). Binding of glucan-binding protein C to GTFD-synthesized soluble glucan in sucrose-dependent adhesion of Streptococcus mutans. Oral Microbiol Immunol 21, 42–46.[CrossRef]
    [Google Scholar]
  18. Monchois, V., Willemot, R. M. & Monsan, P. ( 1999; ). Glucansucrases: mechanism of action and structure-function relationships. FEMS Microbiol Rev 23, 131–151.
    [Google Scholar]
  19. Morris, S., Hanna, S. & Miles, M. J. ( 2004; ). The self-assembly of plant cell wall components by single-molecule force spectroscopy and Monte Carlo modelling. Nanotechnology 15, 1296–1301.[CrossRef]
    [Google Scholar]
  20. O'Toole, G., Kaplan, H. B. & Kolter, R. ( 2000; ). Biofilm formation as microbial development. Annu Rev Microbiol 54, 49–79.[CrossRef]
    [Google Scholar]
  21. Ooshima, T., Matsumura, M., Hoshino, T., Kawabata, S., Sobue, S. & Fujiwara, T. ( 2001; ). Contributions of three glycosyltransferases to sucrose-dependent adherence of Streptococcus mutans. J Dent Res 80, 1672–1677.[CrossRef]
    [Google Scholar]
  22. Pelling, A. E., Sehati, S., Gralla, E. B., Valentine, J. S. & Gimzewski, J. K. ( 2004; ). Local nanomechanical motion of the cell wall of Saccharomyces cerevisiae. Science 305, 1147–1150.[CrossRef]
    [Google Scholar]
  23. Pelling, A. E., Li, Y., Shi, W. & Gimzewski, J. K. ( 2005; ). Nanoscale visualization and characterization of Myxococcus xanthus cells with atomic force microscopy. Proc Natl Acad Sci U S A 102, 6484–6489.[CrossRef]
    [Google Scholar]
  24. Qi, F., Chen, P. & Caufield, P. W. ( 2001; ). The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl Environ Microbiol 67, 15–21.[CrossRef]
    [Google Scholar]
  25. Rief, M., Gautel, M., Oesterhelt, F., Fernandez, J. M. & Gaub, H. E. ( 1997; ). Reversible unfolding of individual titin immunoglobulin domains by AFM. Science 276, 1109–1112.[CrossRef]
    [Google Scholar]
  26. Russell, M. W., Harrington, D. J. & Russell, R. R. ( 1995; ). Identity of Streptococcus mutans surface protein antigen III and wall-associated protein antigen A. Infect Immun 63, 733–735.
    [Google Scholar]
  27. Ryan, V., Hart, T. R. & Schiller, R. ( 1980; ). Laser light scattering measurement of dextran-induced Streptococcus mutans aggregation. Biophys J 31, 113–125.[CrossRef]
    [Google Scholar]
  28. Schär-Zammaretti, P. & Ubbink, J. ( 2003a; ). Imaging of lactic acid bacteria with AFM--elasticity and adhesion maps and their relationship to biological and structural data. Ultramicroscopy 97, 199–208.[CrossRef]
    [Google Scholar]
  29. Schär-Zammaretti, P. & Ubbink, J. ( 2003b; ). The cell wall of lactic acid bacteria: surface constituents and macromolecular conformations. Biophys J 85, 4076–4092.[CrossRef]
    [Google Scholar]
  30. Sen, S., Subramanian, S. & Discher, D. E. ( 2005; ). Indentation and adhesive probing of a cell membrane with AFM: theoretical model and experiments. Biophys J 89, 3203–3213.[CrossRef]
    [Google Scholar]
  31. Smith, B. L., Schaffer, T. E., Viani, M., Thompson, J. B., Frederick, N. A., Kindt, J., Belcher, A., Stucky, G. D., Morse, D. E. & Hansma, P. K. ( 1999; ). Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 399, 761–763.[CrossRef]
    [Google Scholar]
  32. Tsumori, H. & Kuramitsu, H. ( 1997; ). The role of the Streptococcus mutans glucosyltransferases in the sucrose-dependent attachment to smooth surfaces: essential role of the GtfC enzyme. Oral Microbiol Immunol 12, 274–280.[CrossRef]
    [Google Scholar]
  33. van der Aa, B. C., Michel, R. M., Asther, M., Zamora, M. T., Rouxhet, P. G. & Dufrene, Y. F. ( 2001; ). Stretching cell surface macromolecules by atomic force microscopy. Langmuir 17, 3116–3119.[CrossRef]
    [Google Scholar]
  34. van der Mei, H. C., Busscher, H. J., Bos, R., de Vries, J., Boonaert, C. J. & Dufrene, Y. F. ( 2000; ). Direct probing by atomic force microscopy of the cell surface softness of a fibrillated and nonfibrillated oral streptococcal strain. Biophys J 78, 2668–2674.[CrossRef]
    [Google Scholar]
  35. van Hoogmoed, C. G., Dijkstra, R. J. B., van der Mei, H. C. & Busscher, H. J. ( 2006; ). Influence of biosurfactant on interactive forces between mutans streptococci and enamel measured by atomic force microscopy. J Dent Res 85, 54–58.[CrossRef]
    [Google Scholar]
  36. Yamashita, Y., Bowen, W. H., Burne, R. A. & Kuramitsu, H. K. ( 1993; ). Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun 61, 3811–3817.
    [Google Scholar]
  37. Zhu, L., Kreth, J., Cross, S. E., Gimzewski, J. K., Shi, W. Y. & Qi, F. X. ( 2006; ). Functional characterization of cell-wall-associated protein WapA in Streptococcus mutans. Microbiology 152, 2395–2404.[CrossRef]
    [Google Scholar]
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