Abstract
Streptococci and actinomyces that initiate colonization of the tooth surface frequently coaggregate with each other as well as with other oral bacteria. These observations have led to the hypothesis that interbacterial adhesion influences spatiotemporal development of plaque. To assess the role of such interactions in oral biofilm formation in vivo, antibodies directed against bacterial surface components that mediate coaggregation interactions were used as direct immunofluorescent probes in conjunction with laser confocal microscopy to determine the distribution and spatial arrangement of bacteria within intact human plaque formed on retrievable enamel chips. In intrageneric coaggregation, streptococci such as Streptococcus gordonii DL1 recognize receptor polysaccharides (RPS) borne on other streptococci such as Streptococcus oralis 34. To define potentially interactive subsets of streptococci in the developing plaque, an antibody against RPS (anti-RPS) was used together with an antibody against S. gordonii DL1 (anti-DL1). These antibodies reacted primarily with single cells in 4-h-old plaque and with mixed-species microcolonies in 8-h-old plaque. Anti-RPS-reactive bacteria frequently formed microcolonies with anti-DL1-reactive bacteria and with other bacteria distinguished by general nucleic acid stains. In intergeneric coaggregation between streptococci and actinomyces, type 2 fimbriae of actinomyces recognize RPS on the streptococci. Cells reactive with antibody against type 2 fimbriae of Actinomyces naeslundii T14V (anti-type-2) were much less frequent than either subset of streptococci. However, bacteria reactive with anti-type-2 were seen in intimate association with anti-RPS-reactive cells. These results are the first direct demonstration of coaggregation-mediated interactions during initial plaque accumulation in vivo. Further, these results demonstrate the spatiotemporal development and prevalence of mixed-species communities in early dental plaque.
MeSH Terms
Actinomyces/metabolism,physiology
Antibodies, Bacterial/immunology
Bacterial Adhesion
Dental Enamel/microbiology
Dental Plaque/microbiology
Fimbriae, Bacterial/metabolism
Humans
Microscopy, Confocal
Polysaccharides, Bacterial/immunology,metabolism
Receptors, Cell Surface/immunology,metabolism
Streptococcus/metabolism,physiology
Chemicals
Antibodies, Bacterial
Polysaccharides, Bacterial
Receptors, Cell Surface
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Palmer Robert J
National Institute of Dental and Craniofacial Research, National Institutes of Health, Bethesda, Maryland 20892-4350, USA.
Gordon Sharon M
Cisar John O
Kolenbrander Paul E
References (28)
28 references, click to expand
-
Bacterial diversity within the human subgingival crevice.
Proc Natl Acad Sci U S A. 1999 Dec 7;96(25):14547-52
PMID: 10588742
-
Actinomyces serovar WVA963 coaggregation-defective mutant strain PK2407 secretes lactose-sensitive adhesin that binds to coaggregation partner Streptococcus oralis 34.
Oral Microbiol Immunol. 1998 Dec;13(6):337-40
PMID: 9872108
-
A novel technique for monitoring the development of bacterial biofilms in human periodontal pockets.
FEMS Microbiol Lett. 2000 Oct 1;191(1):95-101
PMID: 11004405
-
Retrieval of biofilms from the oral cavity.
Methods Enzymol. 2001;337:393-403
PMID: 11398445
-
Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source.
Infect Immun. 2001 Sep;69(9):5794-804
PMID: 11500457
-
The localization of periodontal-disease-associated bacteria in human periodontal pockets.
J Dent Res. 2001 Oct;80(10):1930-4
PMID: 11706954
-
Molecular analysis of bacterial species associated with childhood caries.
J Clin Microbiol. 2002 Mar;40(3):1001-9
PMID: 11880430
-
The microbial community composition of a nitrifying-denitrifying activated sludge from an industrial sewage treatment plant analyzed by the full-cycle rRNA approach.
Syst Appl Microbiol. 2002 Apr;25(1):84-99
PMID: 12086193
-
Phylogenetic relationships and coaggregation ability of freshwater biofilm bacteria.
Appl Environ Microbiol. 2002 Jul;68(7):3644-50
PMID: 12089055
-
Interbacterial aggregation of plaque bacteria.
Arch Oral Biol. 1970 Dec;15(12):1397-400
PMID: 5280139
-
Specific absence of type 2 fimbriae on a coaggregation-defective mutant of Actinomyces viscosus T14V.
Infect Immun. 1983 May;40(2):759-65
PMID: 6132880
-
Exclusive presence of lactose-sensitive fimbriae on a typical strain (WVU45) of Actinomyces naeslundii.
Infect Immun. 1984 Nov;46(2):453-8
PMID: 6150007
-
Scanning electron microscopy of early microbial colonization of human enamel and root surfaces in vivo.
Scand J Dent Res. 1987 Aug;95(4):287-96
PMID: 3476984
-
Transmission electron microscopy of early microbial colonization of human enamel and root surfaces in vivo.
Scand J Dent Res. 1987 Aug;95(4):297-307
PMID: 3306888
-
Microbiology of the early colonization of human enamel and root surfaces in vivo.
Scand J Dent Res. 1987 Oct;95(5):369-80
PMID: 3477852
-
A polysaccharide from Streptococcus sanguis 34 that inhibits coaggregation of S. sanguis 34 with Actinomyces viscosus T14V.
J Bacteriol. 1988 May;170(5):2229-35
PMID: 3360742
-
Adsorbed salivary proline-rich protein 1 and statherin: receptors for type 1 fimbriae of Actinomyces viscosus T14V-J1 on apatitic surfaces.
Infect Immun. 1988 Nov;56(11):2990-3
PMID: 2902013
-
Actinomyces georgiae sp. nov., Actinomyces gerencseriae sp. nov., designation of two genospecies of Actinomyces naeslundii, and inclusion of A. naeslundii serotypes II and III and Actinomyces viscosus serotype II in A. naeslundii genospecies 2.
Int J Syst Bacteriol. 1990 Jul;40(3):273-86
PMID: 2397195
-
Comparison of the initial streptococcal microflora on dental enamel in caries-active and in caries-inactive individuals.
Caries Res. 1990;24(4):267-72
PMID: 2276164
-
Intrageneric coaggregation among strains of human oral bacteria: potential role in primary colonization of the tooth surface.
Appl Environ Microbiol. 1990 Dec;56(12):3890-4
PMID: 2082831
-
Microbial colonization of human tooth surfaces.
APMIS Suppl. 1993;32:1-45
PMID: 8494649
-
Adhere today, here tomorrow: oral bacterial adherence.
J Bacteriol. 1993 Jun;175(11):3247-52
PMID: 8501028
-
Lectin recognition of host-like saccharide motifs in streptococcal cell wall polysaccharides.
Glycobiology. 1995 Oct;5(7):655-62
PMID: 8608267
-
Structural and antigenic types of cell wall polysaccharides from viridans group streptococci with receptors for oral actinomyces and streptococcal lectins.
Infect Immun. 1997 Dec;65(12):5035-41
PMID: 9393793
-
Developmental biology of biofilms: implications for treatment and control.
Trends Microbiol. 1997 Nov;5(11):435-40
PMID: 9402699
-
Scanning electron microscopy of microbial colonization of 'rapid' and 'slow' dental-plaque formers in vivo.
Arch Oral Biol. 1997 Oct-Nov;42(10-11):735-42
PMID: 9447263
-
Fluorescence in situ hybridization shows spatial distribution of as yet uncultured treponemes in biopsies from digital dermatitis lesions.
Microbiology. 1998 Sep;144 ( Pt 9):2459-67
PMID: 9782493
-
Coaggregation between aquatic bacteria is mediated by specific-growth-phase-dependent lectin-saccharide interactions.
Appl Environ Microbiol. 2000 Jan;66(1):431-4
PMID: 10618261