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. 1995 Dec;63(12):4584–4588. doi: 10.1128/iai.63.12.4584-4588.1995

Intergeneric coaggregation of oral Treponema spp. with Fusobacterium spp. and intrageneric coaggregation among Fusobacterium spp.

P E Kolenbrander 1, K D Parrish 1, R N Andersen 1, E P Greenberg 1
PMCID: PMC173658  PMID: 7591109

Abstract

A total of 22 strains of Treponema spp. including members of all four named human oral species were tested for coaggregation with 7 strains of oral fusobacteria, 2 strains of nonoral fusobacteria, and 45 strains of other oral bacteria, which included actinobacilli, actinomyces, capnocytophagae, eubacteria, porphyromonads, prevotellae, selenomonads, streptococci, and veillonellae. None of the treponemes coaggregated with any of the latter 45 oral strains or with the two nonoral fusobacteria. All treponemes, eight Treponema denticola strains, eight T. socranskii strains, four oral pectinolytic treponemes, one T. pectinovorum strain, and one T. vincentii strain coaggregated with at least one strain of the fusobacteria tested as partners. The partners consisted of one strain of Fusobacterium periodonticum, five F. nucleatum strains including all four subspecies of F. nucleatum, and a strain of F. simiae obtained from the dental plaque of a monkey. In the more than 100 coaggregations observed, the fusobacterial partner was heat inactivated (85 degrees C for 30 min), while the treponemes were unaffected by the heat treatment. Furthermore, the fusobacteria were usually inactivated by proteinase K treatment, and the treponemes were not affected. Only the T. denticola coaggregations were inhibited by lactose and D-galactosamine. None were inhibited by any of 23 other different sugars or L-arginine. Intragenic coaggregations were seen among the subspecies of F. nucleatum and with F. periodonticum, and none were inhibited by any of the sugars tested or by L-arginine. No intrageneric coaggregations were observed among the treponemes. These data indicate that the human oral treponemes show a specificity for oral fusobacteria as coaggregation partners. Such cell-to cell contact may facilitate efficient metabolic communication and enhance the proliferation of each cell in the progressively more severe stages of periodontal disease.

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Selected References

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  1. Breznak J. A., Pankratz H. S. In situ morphology of the gut microbiota of wood-eating termites [Reticulitermes flavipes (Kollar) and Coptotermes formosanus Shiraki]. Appl Environ Microbiol. 1977 Feb;33(2):406–426. doi: 10.1128/aem.33.2.406-426.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Carlsson J., Larsen J. T., Edlund M. B. Utilization of glutathione (L-gamma-glutamyl-L-cysteinylglycine) by Fusobacterium nucleatum subspecies nucleatum. Oral Microbiol Immunol. 1994 Oct;9(5):297–300. doi: 10.1111/j.1399-302x.1994.tb00074.x. [DOI] [PubMed] [Google Scholar]
  3. Cavedon K., London J. Adhesin degradation: a possible function for a Prevotella loescheii protease? Oral Microbiol Immunol. 1993 Oct;8(5):283–287. doi: 10.1111/j.1399-302x.1993.tb00575.x. [DOI] [PubMed] [Google Scholar]
  4. Ciborowski P., Nishikata M., Allen R. D., Lantz M. S. Purification and characterization of two forms of a high-molecular-weight cysteine proteinase (porphypain) from Porphyromonas gingivalis. J Bacteriol. 1994 Aug;176(15):4549–4557. doi: 10.1128/jb.176.15.4549-4557.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cisar J. O., Kolenbrander P. E., McIntire F. C. Specificity of coaggregation reactions between human oral streptococci and strains of Actinomyces viscosus or Actinomyces naeslundii. Infect Immun. 1979 Jun;24(3):742–752. doi: 10.1128/iai.24.3.742-752.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dzink J. L., Sheenan M. T., Socransky S. S. Proposal of three subspecies of Fusobacterium nucleatum Knorr 1922: Fusobacterium nucleatum subsp. nucleatum subsp. nov., comb. nov.; Fusobacterium nucleatum subsp. polymorphum subsp. nov., nom. rev., comb. nov.; and Fusobacterium nucleatum subsp. vincentii subsp. nov., nom. rev., comb. nov. Int J Syst Bacteriol. 1990 Jan;40(1):74–78. doi: 10.1099/00207713-40-1-74. [DOI] [PubMed] [Google Scholar]
  7. Ellen R. P., Dawson J. R., Yang P. F. Treponema denticola as a model for polar adhesion and cytopathogenicity of spirochetes. Trends Microbiol. 1994 Apr;2(4):114–119. doi: 10.1016/0966-842x(94)90597-5. [DOI] [PubMed] [Google Scholar]
  8. Falkler W. A., Jr, Smoot C. N., Mongiello J. R. Attachment of cell fragments of Fusobacterium nucleatum to oral epithelial cells, gingival fibroblasts and white blood cells. Arch Oral Biol. 1982;27(7):553–559. doi: 10.1016/0003-9969(82)90069-3. [DOI] [PubMed] [Google Scholar]
  9. Geesey G. G., Richardson W. T., Yeomans H. G., Irvin R. T., Costerton J. W. Microscopic examination of natural sessile bacterial populations from an alpine stream. Can J Microbiol. 1977 Dec;23(12):1733–1736. doi: 10.1139/m77-249. [DOI] [PubMed] [Google Scholar]
  10. Grenier D. Demonstration of a bimodal coaggregation reaction between Porphyromonas gingivalis and Treponema denticola. Oral Microbiol Immunol. 1992 Oct;7(5):280–284. doi: 10.1111/j.1399-302x.1992.tb00589.x. [DOI] [PubMed] [Google Scholar]
  11. Haffajee A. D., Socransky S. S. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000. 1994 Jun;5:78–111. doi: 10.1111/j.1600-0757.1994.tb00020.x. [DOI] [PubMed] [Google Scholar]
  12. Jansen H. J., van der Hoeven J. S., van den Kieboom C. W., Göertz J. H., Camp P. J., Bakkeren J. A. Degradation of immunoglobulin G by periodontal bacteria. Oral Microbiol Immunol. 1994 Dec;9(6):345–351. doi: 10.1111/j.1399-302x.1994.tb00284.x. [DOI] [PubMed] [Google Scholar]
  13. Kolenbrander P. E., Andersen R. N. Characterization of Streptococcus gordonii (S. sanguis) PK488 adhesin-mediated coaggregation with Actinomyces naeslundii PK606. Infect Immun. 1990 Sep;58(9):3064–3072. doi: 10.1128/iai.58.9.3064-3072.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kolenbrander P. E., Andersen R. N. Inhibition of coaggregation between Fusobacterium nucleatum and Porphyromonas (Bacteroides) gingivalis by lactose and related sugars. Infect Immun. 1989 Oct;57(10):3204–3209. doi: 10.1128/iai.57.10.3204-3209.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kolenbrander P. E., Andersen R. N., Moore L. V. Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect Immun. 1989 Oct;57(10):3194–3203. doi: 10.1128/iai.57.10.3194-3203.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kolenbrander P. E., London J. Adhere today, here tomorrow: oral bacterial adherence. J Bacteriol. 1993 Jun;175(11):3247–3252. doi: 10.1128/jb.175.11.3247-3252.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kuramitsu H. K., Yoneda M., Madden T. Proteases and collagenases of Porphyromonas gingivalis. Adv Dent Res. 1995 Feb;9(1):37–40. doi: 10.1177/08959374950090010701. [DOI] [PubMed] [Google Scholar]
  18. Moore W. E., Moore L. V. The bacteria of periodontal diseases. Periodontol 2000. 1994 Jun;5:66–77. doi: 10.1111/j.1600-0757.1994.tb00019.x. [DOI] [PubMed] [Google Scholar]
  19. Murray P. A., Kern D. G., Winkler J. R. Identification of a galactose-binding lectin on Fusobacterium nucleatum FN-2. Infect Immun. 1988 May;56(5):1314–1319. doi: 10.1128/iai.56.5.1314-1319.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Mäkinen K. K., Mäkinen P. L., Loesche W. J., Syed S. A. Purification and general properties of an oligopeptidase from Treponema denticola ATCC 35405--a human oral spirochete. Arch Biochem Biophys. 1995 Feb 1;316(2):689–698. doi: 10.1006/abbi.1995.1092. [DOI] [PubMed] [Google Scholar]
  21. Potts T. V., Holdeman L. V., Slots J. Relationships among the oral fusobacteria assessed by DNA-DNA hybridization. J Dent Res. 1983 Jun;62(6):702–705. doi: 10.1177/00220345830620060101. [DOI] [PubMed] [Google Scholar]
  22. Reid G., McGroarty J. A., Angotti R., Cook R. L. Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can J Microbiol. 1988 Mar;34(3):344–351. doi: 10.1139/m88-063. [DOI] [PubMed] [Google Scholar]
  23. Reijntjens F. M., Mikx F. H., Wolters-Lutgerhorst J. M., Maltha J. C. Adherence of oral treponemes and their effect on morphological damage and detachment of epithelial cells in vitro. Infect Immun. 1986 Feb;51(2):642–647. doi: 10.1128/iai.51.2.642-647.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Robert J. C., Bonnaure-Mallet M., Florent C., Cloche D. Use of scanning electron microscopy to investigate dental calculus in dogs. Vet Rec. 1990 Nov 10;127(19):475–477. [PubMed] [Google Scholar]
  25. Robert J. C., Bonnaure-Mallet M. Types de coagrégations interbactériennes dans la plaque dentaire. Actual Odontostomatol (Paris) 1990 Dec;(172):697–707. [PubMed] [Google Scholar]
  26. Rogers A. H., Gully N. J., Pfennig A. L., Zilm P. S. The breakdown and utilization of peptides by strains of Fusobacterium nucleatum. Oral Microbiol Immunol. 1992 Oct;7(5):299–303. doi: 10.1111/j.1399-302x.1992.tb00592.x. [DOI] [PubMed] [Google Scholar]
  27. Seow W. K., Seymour G. J., Thong Y. H. Direct modulation of human neutrophil adherence by coaggregating periodontopathic bacteria. Int Arch Allergy Appl Immunol. 1987;83(2):121–128. doi: 10.1159/000234344. [DOI] [PubMed] [Google Scholar]
  28. Takemoto T., Ozaki M., Shirakawa M., Hino T., Okamoto H. Purification of arginine-sensitive hemagglutinin from Fusobacterium nucleatum and its role in coaggregation. J Periodontal Res. 1993 Jan;28(1):21–26. doi: 10.1111/j.1600-0765.1993.tb01046.x. [DOI] [PubMed] [Google Scholar]
  29. Tuttle R. S., Mangan D. F. Interaction of Fusobacterium nucleatum 191 with human peripheral blood lymphocytes. J Periodontal Res. 1990 Nov;25(6):364–371. doi: 10.1111/j.1600-0765.1990.tb00929.x. [DOI] [PubMed] [Google Scholar]
  30. Vandevoorde L., Christiaens H., Verstraete W. Prevalence of coaggregation reactions among chicken lactobacilli. J Appl Bacteriol. 1992 Mar;72(3):214–219. doi: 10.1111/j.1365-2672.1992.tb01826.x. [DOI] [PubMed] [Google Scholar]
  31. Weber F. H., Canale-Parola E. Pectinolytic enzymes of oral spirochetes from humans. Appl Environ Microbiol. 1984 Jul;48(1):61–67. doi: 10.1128/aem.48.1.61-67.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. ter Steeg P. F., van der Hoeven J. S. Growth stimulation of Treponema denticola by periodontal microorganisms. Antonie Van Leeuwenhoek. 1990 Feb;57(2):63–70. doi: 10.1007/BF00403156. [DOI] [PubMed] [Google Scholar]

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