1887

Abstract

is an aggressive periodontal pathogen that persists in the mixed-species plaque biofilm on tooth surfaces. cells attach to the plaque commensal and this coadhesion event leads to the development of biofilms. Binding of these organisms is multimodal, involving both the major fimbrial FimA protein and the species-specific interaction of the minor fimbrial Mfa1 protein with the streptococcal SspB protein. This study examined the contribution of the Mfa1–SspB interaction to biofilm formation. biofilms readily formed on substrata of DL1 but not on cells which lack a coadhesion-mediating homologue of SspB. An insertional inactivation of the gene in resulted in a phenotype deficient in binding and unable to form biofilms. Furthermore, analysis using recombinant streptococci and enterococci showed that biofilms formed on strains expressing SspB or translational fusions of SspB with SpaP (the non-adherent SspB homologue in ) containing the adherence domain (Ssp dherence egion, BAR) of SspB. In contrast, an isogenic Ssp null mutant of DL1 was unable to support biofilm growth, even though this strain bound to FimA at levels similar to wild-type DL1. Finally, site-specific mutation of two functional amino acid residues in BAR resulted in SspB polypeptides that did not promote the development of biofilms. These results suggest that the induction of biofilms on a streptococcal substrate requires functional SspB–minor fimbriae interactions.

Loading

Article metrics loading...

/content/journal/micro/10.1099/00221287-148-6-1627
2002-06-01
2020-04-01
Loading full text...

Full text loading...

/deliver/fulltext/micro/148/6/1481627a.html?itemId=/content/journal/micro/10.1099/00221287-148-6-1627&mimeType=html&fmt=ahah

References

  1. Arai M., Hamada N., Umemoto T. 2000; Purification and characterization of a novel secondary fimbrial protein from Porphyromonas gingivalis strain 381. FEMS Microbiol Lett93:75–81
    [Google Scholar]
  2. Belton C. M., Izutsu K. T., Goodwin P. C., Park Y., Lamont R. J. 1999; Fluorescence image analysis of the association between Porphyromonas gingivalis and gingival epithelial cells. Cell Microbiol1:215–224[CrossRef]
    [Google Scholar]
  3. Bradshaw D. J., Marsh P. D., Watson G. K., Allison C. 1998; Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect Immun66:4729–4732
    [Google Scholar]
  4. Brooks W., Demuth D. R., Gil S., Lamont R. J. 1997; Identification of a Streptococcus gordonii SspB domain that mediates adhesion to Porphyromonas gingivalis . Infect Immun65:3753–3758
    [Google Scholar]
  5. Chung W. O., Demuth D. R., Lamont R. J. 2000; Identification of a Porphyromonas gingivalis receptor for the Streptococcus gordonii SspB protein. Infect Immun68:6758–6762[CrossRef]
    [Google Scholar]
  6. Chung W. O., Park Y., Lamont R. J., McNab R., Barbieri B., Demuth D. R. 2001; Signaling system in Porphyromonas gingivalis based on a LuxS protein. J Bacteriol183:3903–3909[CrossRef]
    [Google Scholar]
  7. Cleary P., Retnoningrum D. 1994; Group A streptococcal immunoglobulin-binding proteins: adhesins, molecular mimicry or sensory proteins?. Trends Microbiol2:131–136[CrossRef]
    [Google Scholar]
  8. Cook G. S., Costerton J. W., Lamont R. J. 1998; Biofilm formation by Porphyromonas gingivalis and Streptococcus gordonii . J Periodontol Res33:323–327[CrossRef]
    [Google Scholar]
  9. Cornelis G., Van Gijsegem F. 2000; Assembly and function of type III secretory systems. Annu Rev Microbiol54:735–774[CrossRef]
    [Google Scholar]
  10. Curtis M. A., Kuramitsu H. K., Lantz M., Macrina F. L., Nakayama K., Potempa J., Reynolds E. C., Aduse-Opoku J. 1999; Molecular genetics and nomenclature of proteases of Porphyromonas gingivalis . J Periodontol Res34:464–472[CrossRef]
    [Google Scholar]
  11. Davies D. G., Parsek M. R., Pearson J. P., Iglewski B. H., Costerton J. W., Greenberg E. P. 1998; The involvement of cell-to-cell signals in the development of a bacterial biofilm. Science280:295–298[CrossRef]
    [Google Scholar]
  12. Demuth D. R., Berthold P., Leboy P. S., Golub E. E., Davis C. A., Malamud D. 1989; Saliva-mediated aggregation of Enterococcus faecalis transformed with a Streptococcus sanguis gene encoding the SSP-5 surface antigen. Infect Immun57:1470–1475
    [Google Scholar]
  13. Demuth D. R., Duan Y., Brooks W., Holmes A. R., McNab R., Jenkinson H. F. 1996; Tandem genes encode cell-surface polypeptides SspA and SspB which mediate adhesion of the oral bacterium Streptococcus gordonii to human and bacterial receptors. Mol Microbiol20:403–413[CrossRef]
    [Google Scholar]
  14. Demuth D. R., Irvine D. C., Costerton J. W., Cook G. S., Lamont R. J. 2001; Discrete protein determinant directs the species-specific adherence of Porphyromonas gingivalis to oral streptococci. Infect Immun69:5736–5741[CrossRef]
    [Google Scholar]
  15. Guggenheim M., Shapiro S., Gmur R., Guggenheim B. 2001; Spatial arrangements and associative behavior of species in an in vitro oral biofilm model. Appl Environ Microbiol67:1343–1350[CrossRef]
    [Google Scholar]
  16. Hamada N., Sojar H. T., Cho M.-I., Genco R. J. 1996; Isolation and characterization of a minor fimbria from Porphyromonas gingivalis . Infect Immun64:4788–4794
    [Google Scholar]
  17. Hayashi J., Nishikawa K., Hirano R., Noguchi T., Yoshimura F. 2000; Identification of a two-component signal transduction system involved in fimbriation of Porphyromonas gingivalis . Microbiol Immunol44:279–282[CrossRef]
    [Google Scholar]
  18. Jenkinson H. F., Demuth D. R. 1997; Structure, function and immunogenicity of streptococcal antigen I/II polypeptides. Mol Microbiol23:183–190[CrossRef]
    [Google Scholar]
  19. Jenkinson H. F., Terry S. D., McNab R., Tannock G. W. 1993; Inactivation of the gene encoding surface protein SspA in Streptococcus gordonii DL1 affects cell interactions with human salivary agglutinin and oral actinomyces. Infect Immun61:3199–3208
    [Google Scholar]
  20. Kinder S. A., Holt S. C. 1989; Characterization of coaggregation between Bacteroides gingivalis T22 and Fusobacterium nucleatum T18. Infect Immun57:3425–3433
    [Google Scholar]
  21. Kolenbrander P. E., Andersen R. N. 1989; Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas ( Bacteroides ) gingivalis by lactose and related sugars. Infect Immun57:3204–3209
    [Google Scholar]
  22. Kolenbrander P. E., London J. 1993; Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol175:3247–3252
    [Google Scholar]
  23. Lamont R. J., Jenkinson H. F. 1998; Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis . Microbiol Mol Biol Rev62:1244–1263
    [Google Scholar]
  24. Lamont R. J., Jenkinson H. F. 2000; Subgingival colonization by Porphyromonas gingivalis . Oral Microbiol Immunol15:341–349[CrossRef]
    [Google Scholar]
  25. Lamont R. J., Hersey S. G., Rosan B. 1992; Characterization of the adherence of Porphyromonas ( Bacteroides ) gingivalis to oral streptococci. Oral Microbiol Immunol7:193–197[CrossRef]
    [Google Scholar]
  26. Lamont R. J., Bevan C. A., Gil S., Persson R. E., Rosan B. 1993; Involvement of Porphyromonas gingivalis fimbriae in adherence to Streptococcus gordonii. Oral Microbiol Immunol8:272–276[CrossRef]
    [Google Scholar]
  27. Lamont R. J., Chan A., Belton C. M., Izutsu K. T., Vasel D., Weinberg A. 1995; Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun63:3878–3885
    [Google Scholar]
  28. Lee S. W., Hillman J. D., Progulske-Fox A. 1996; The hemagglutinin genes hagG and hagC of Porphyromonas gingivalis are transcribed in vivo as shown by the use of a new expression vector. Infect Immun64:4802–4810
    [Google Scholar]
  29. Love R. M., McMillan M. D., Park Y., Jenkinson H. F. 2000; Coinvasion of dentinal tubules by Porphyromonas gingivalis and Streptococcus gordonii depends upon binding specificity of streptococcal antigen I/II adhesin. Infect Immun68:1359–1365[CrossRef]
    [Google Scholar]
  30. Marsh P. D. 1989; Host defenses and microbial homeostasis: role of microbial interactions. J Dent Res68:1567–1575
    [Google Scholar]
  31. Marsh P. D. 1994; Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res8:263–271
    [Google Scholar]
  32. McNab R., Jenkinson H. F. 1998; Altered adherence properties of a Streptococcus gordonii hppA (oligopeptide permease) mutant result from transcriptional effects on cshA adhesin gene expression. Microbiology144:127–136[CrossRef]
    [Google Scholar]
  33. Park Y., Lamont R. J. 1998; Contact-dependent protein secretion in Porphyromonas gingivalis . Infect Immun66:4777–4782
    [Google Scholar]
  34. Rosan B., Lamont R. J. 2000; Dental plaque formation. Microbes Infect2:1599–1607[CrossRef]
    [Google Scholar]
  35. Scannapieco F. A. 1994; Saliva-bacterium interactions in oral microbial ecology. Crit Rev Oral Biol Med5:203–248
    [Google Scholar]
  36. Schwarz S., Ellen R. P., Grove D. A. 1987; Bacteroides gingivalis - Actinomyces viscosus cohesive interactions as measured by a quantitative binding assay. Infect Immun55:2391–2397
    [Google Scholar]
  37. Shaniztki B., Hurwitz D., Smorodinsky N., Ganeshkumar N., Weiss E. I. 1997; Identification of a Fusobacterium nucleatum PK1594 galactose-binding adhesin which mediates coaggregation with periopathogenic bacteria and hemagglutination. Infect Immun65:5231–5237
    [Google Scholar]
  38. Socransky S. S., Haffajee A. D. 1992; The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol63:322–331[CrossRef]
    [Google Scholar]
  39. Travis J., Banbula A., Potempa J. 2000; The role of bacterial and host proteinases in periodontal disease. Adv Exp Med Biol477:455–465
    [Google Scholar]
  40. Wirth R., An F. Y., Clewell D. B. 1986; Highly efficient protoplast transformation system for Streptococcus faecalis and a new Escherichia coli - S. faecalis shuttle vector. J Bacteriol165:831–836
    [Google Scholar]
  41. Xie H., Chung W. O., Park Y., Lamont R. J. 2000; Regulation of the Porphyromonas gingivalis fimA (fimbrillin) gene. Infect Immun68:6574–6579[CrossRef]
    [Google Scholar]
  42. Yao E. S., Lamont R. J., Leu S. P., Weinberg A. 1996; Interbacterial binding among strains of pathogenic and commensal oral bacterial species. Oral Microbiol Immunol11:35–41[CrossRef]
    [Google Scholar]
  43. Yoshimura F., Takashi K., Nodasaka Y., Suzuki T. 1984; Purification and characterization of a novel type of fimbriae from the oral anaerobe Bacteroides gingivalis . J Bacteriol160:949–957
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/00221287-148-6-1627
Loading
/content/journal/micro/10.1099/00221287-148-6-1627
Loading

Data & Media loading...

Most cited this month

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error