Oral multispecies biofilm development and the key role of cell–cell distance (original) (raw)

• Achtman, M. & Wagner, M. Microbial diversity and the genetic nature of microbial species. Nature Rev. Microbiol. 6, 431–440 (2008).
  Article CAS Google Scholar
• Huber, J. A. et al. Effect of PCR amplicon size on assessments of clone library microbial diversity and community structure. Environ. Microbiol. 11, 1292–1302 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Lozupone, C. A. & Knight, R. Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev. 32, 557–578 (2008).
  Article CAS PubMed Google Scholar
• Paster, B. J., Olsen, I., Aas, J. A. & Dewhirst, F. E. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol. 2000 42, 80–87 (2006).
  Article PubMed Google Scholar
• Zaura, E., Keijser, B. J., Huse, S. M. & Crielaard, W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 9, 259 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Xie, H., Lin, X., Wang, B. Y., Wu, J. & Lamont, R. J. Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153, 3228–3234 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Mager, D. L., Ximenez-Fyvie, L. A., Haffajee, A. D. & Socransky, S. S. Distribution of selected bacterial species on intraoral surfaces. J. Clin. Periodontol. 30, 644–654 (2003).
  Article PubMed Google Scholar
• Bos, R., van der Mei, H. C. & Busscher, H. J. Co-adhesion of oral microbial pairs under flow in the presence of saliva and lactose. J. Dent. Res. 75, 809–815 (1996).
  Article CAS PubMed Google Scholar
• Kolenbrander, P. E. & London, J. Adhere today, here tomorrow: oral bacterial adherence. J. Bacteriol. 175, 3247–3252 (1993).
  Article CAS PubMed PubMed Central Google Scholar
• Ledder, R. G., Timperley, A. S., Friswell, M. K., Macfarlane, S. & McBain, A. J. Coaggregation between and among human intestinal and oral bacteria. FEMS Microbiol. Ecol. 66, 630–636 (2008).
  Article CAS PubMed Google Scholar
• Min, K. R. & Rickard, A. H. Coaggregation by the freshwater bacterium Sphingomonas natatoria alters dual-species biofilm formation. Appl. Environ. Microbiol. 75, 3987–3997 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rickard, A. H., Gilbert, P., High, N. J., Kolenbrander, P. E. & Handley, P. S. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 11, 94–100 (2003).
  Article CAS PubMed Google Scholar
• Diaz, P. I. et al. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72, 2837–2848 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Dige, I., Nilsson, H., Kilian, M. & Nyvad, B. In situ identification of streptococci and other bacteria in initial dental biofilm by confocal laser scanning microscopy and fluorescence in situ hybridization. Eur. J. Oral Sci. 115, 459–467 (2007).
  Article PubMed Google Scholar
• Dige, I., Nyengaard, J. R., Kilian, M. & Nyvad, B. Application of stereological principles for quantification of bacteria in intact dental biofilms. Oral Microbiol. Immunol. 24, 69–75 (2009).
  Article CAS PubMed Google Scholar
• Dige, I., Raarup, M. K., Nyengaard, J. R., Kilian, M. & Nyvad, B. Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155, 2116–2126 (2009).
  Article CAS PubMed Google Scholar
• Nyvad, B. & Kilian, M. Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand. J. Dent Res. 95, 369–380 (1987).
  CAS PubMed Google Scholar
• Nyvad, B. & Kilian, M. Comparison of the initial streptococcal microflora on dental enamel in caries-active and in caries-inactive individuals. Caries Res. 24, 267–272 (1990).
  Article CAS PubMed Google Scholar
• Ding, A. M., Palmer, R. J. Jr, Cisar, J. O. & Kolenbrander, P. E. Shear-enhanced oral microbial adhesion. Appl. Environ. Microbiol. 76, 1294–1297 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Chalmers, N. I., Palmer, R. J. Jr, Cisar, J. O. & Kolenbrander, P. E. Characterization of a Streptococcus sp-Veillonella sp. community micromanipulated from dental plaque. J. Bacteriol. 190, 8145–8154 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Chalmers, N. I. et al. Use of quantum dot luminescent probes to achieve single-cell resolution of human oral bacteria in biofilms. Appl. Environ. Microbiol. 73, 630–636 (2007).
  Article CAS PubMed Google Scholar
• Jakubovics, N. S., Gill, S. R., Iobst, S. E., Vickerman, M. M. & Kolenbrander, P. E. Regulation of gene expression in a mixed-genus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J. Bacteriol. 190, 3646–3657 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Jakubovics, N. S., Gill, S. R., Vickerman, M. M. & Kolenbrander, P. E. Role of hydrogen peroxide in competition and cooperation between Streptococcus gordonii and Actinomyces naeslundii. FEMS Microbiol. Ecol. 66, 637–644 (2008).
  Article CAS PubMed Google Scholar
• Palmer, R. J. Jr, Diaz, P. I. & Kolenbrander, P. E. Rapid succession within the Veillonella population of a developing human oral biofilm in situ. J. Bacteriol. 188, 4117–4124 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Palmer, R. J. Jr, Gordon, S. M., Cisar, J. O. & Kolenbrander, P. E. Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J. Bacteriol. 185, 3400–3409 (2003).
  Article CAS PubMed Google Scholar
• Palmer, R. J. Jr, Kazmerzak, K., Hansen, M. C. & Kolenbrander, P. E. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect. Immun. 69, 5794–5804 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Periasamy, S., Chalmers, N. I., Du-Thumm, L. & Kolenbrander, P. E. Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATCC 43146 for growth on saliva in a three-species community that includes Streptococcus oralis 34. Appl. Environ. Microbiol. 75, 3250–3257 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Periasamy, S. & Kolenbrander, P. E. Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities in saliva with Fusobacterium nucleatum and Veillonella sp. Infect. Immun. 77, 3542–3551 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Rickard, A. H., Campagna, S. R. & Kolenbrander, P. E. Autoinducer-2 is produced in saliva-fed flow conditions relevant to natural oral biofilms. J. Appl. Microbiol. 105, 2096–2103 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Rickard, A. H. et al. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60, 1446–1456 (2006).
  Article CAS PubMed Google Scholar
• Periasamy, S. & Kolenbrander, P. E. Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J. Bacteriol. 191, 6804–6811 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Periasamy, S. & Kolenbrander, P. E. Central role of early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle and late colonizers of enamel. J. Bacteriol. 192, 12 Feb 2010 (doi:10.1128/JB.01631-09).
  Article CAS PubMed PubMed Central Google Scholar
• Kaplan, C. W., Lux, R., Haake, S. K. & Shi, W. The Fusobacterium nucleatum outer membrane protein RadD is an arginine-inhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol. 71, 35–47 (2009).
  Article CAS PubMed Google Scholar
• Buckley, M. R. Microbial communities: from life apart to life together. American Academy of Microbiology [online] (2002).
• Diggle, S. P., Gardner, A., West, S. A. & Griffin, A. S. Evolutionary theory of bacterial quorum sensing: when is a signal not a signal? Philos. Trans. R. Soc. Lond. B Biol. Sci. 362, 1241–1249 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Hardie, K. R. & Heurlier, K. Establishing bacterial communities by 'word of mouth': LuxS and autoinducer 2 in biofilm development. Nature Rev. Microbiol. 6, 635–643 (2008).
  Article CAS Google Scholar
• Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249–258 (2006).
  Article CAS Google Scholar
• Redfield, R. J. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365–370 (2002).
  Article CAS PubMed Google Scholar
• Bassler, B. L., Greenberg, E. P. & Stevens, A. M. Cross-species induction of luminescence in the quorum-sensing bacterium Vibrio harveyi. J. Bacteriol. 179, 4043–4045 (1997).
  Article CAS PubMed PubMed Central Google Scholar
• Cosseau, C. et al. The commensal Streptococcus salivarius K12 downregulates the innate immune responses of human epithelial cells and promotes host-microbe homeostasis. Infect. Immun. 76, 4163–4175 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Handfield, M. et al. Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell. Microbiol. 7, 811–823 (2005).
  Article CAS PubMed Google Scholar
• Hasegawa, Y. et al. Gingival epithelial cell transcriptional responses to commensal and opportunistic oral microbial species. Infect. Immun. 75, 2540–2547 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Paddick, J. S., Brailsford, S. R., Kidd, E. A. M. & Beighton, D. Phenotypic and genotypic selection of microbiota surviving under dental restorations. Appl. Environ. Microbiol. 71, 2467–2472 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Wickstrom, C. & Svensater, G. Salivary gel-forming mucin MUC5B - a nutrient for dental plaque bacteria. Oral Microbiol. Immunol. 23, 177–182 (2008).
  Article CAS PubMed Google Scholar
• Dawes, C. What is the critical pH and why does a tooth dissolve in acid? J. Can. Dent. Assoc. 69, 722–724 (2003).
  PubMed Google Scholar
• de Soet, J. J., Nyvad, B. & Kilian, M. Strain-related acid production by oral streptococci. Caries Res. 34, 486–490 (2000).
  Article CAS PubMed Google Scholar
• Burne, R. A. & Marquis, R. E. Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol. Lett. 193, 1–6 (2000).
  Article CAS PubMed Google Scholar
• Marsh, P. D. Are dental diseases examples of ecological catastrophes? Microbiology 149, 279–294 (2003).
  Article CAS PubMed Google Scholar
• Becker, M. R. et al. Molecular analysis of bacterial species associated with childhood caries. J. Clin. Microbiol. 40, 1001–1009 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Lo, E. C., Schwarz, E. & Wong, M. C. Arresting dentine caries in Chinese preschool children. Int. J. Paediatr. Dent. 8, 253–260 (1998).
  Article CAS PubMed Google Scholar
• Dixon, D. R., Reife, R. A., Cebra, J. J. & Darveau, R. P. Commensal bacteria influence innate status within gingival tissues: a pilot study. J. Periodontol. 75, 1486–1492 (2004).
  Article PubMed Google Scholar
• Socransky, S. S., Smith, C. & Haffajee, A. D. Subgingival microbial profiles in refractory periodontal disease. J. Clin. Periodontol. 29, 260–268 (2002).
  Article PubMed Google Scholar
• Haffajee, A. D., Teles, R. P. & Socransky, S. S. The effect of periodontal therapy on the composition of the subgingival microbiota. Periodontol. 2000 42, 219–258 (2006).
  Article PubMed Google Scholar
• Kilic, A. O. et al. Involvement of Streptococcus gordonii b-glucoside metabolism systems in adhesion, biofilm formation, and in vivo gene expression. J. Bacteriol. 186, 4246–4253 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Merritt, J., Niu, G., Okinaga, T. & Qi, F. Autoaggregation response of Fusobacterium nucleatum. Appl. Environ. Microbiol. 75, 7725–7733 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Stadtman, E. R. & Levine, R. L. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25, 207–218 (2003).
  Article CAS PubMed Google Scholar
• Kreth, J., Zhang, Y. & Herzberg, M. C. Streptococcal antagonism in oral biofilms: Streptococcus sanguinis and Streptococcus gordonii interference with Streptococcus mutans. J. Bacteriol. 190, 4632–4640 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Kuboniwa, M. et al. Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol. 9, 98 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Simionato, M. R. et al. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74, 6419–6428 (2006).
  Article CAS PubMed PubMed Central Google Scholar
• Egland, P. G., Palmer, R. J. Jr & Kolenbrander, P. E. Interspecies communication in _Streptococcus gordonii_-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc. Natl Acad. Sci. USA 101, 16917–16922 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Johnson, B. P. et al. Interspecies signaling between Veillonella atypica and Streptococcus gordonii requires the transcription factor CcpA. J. Bacteriol. 191, 5563–5565 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Bamford, C. V. et al. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 77, 3696–3704 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Samaranayake, L. P., Keung Leung, W. & Jin, L. Oral mucosal fungal infections. Periodontol. 2000 49, 39–59 (2009).
  Article PubMed Google Scholar
• Xavier, K. B. et al. Phosphorylation and processing of the quorum-sensing molecule autoinducer-2 in enteric bacteria. ACS Chem. Biol. 2, 128–136 (2007).
  Article CAS PubMed Google Scholar
• Ahmed, N. A., Petersen, F. C. & Scheie, A. A. AI-2/LuxS is involved in increased biofilm formation by Streptococcus intermedius in the presence of antibiotics. Antimicrob. Agents Chemother. 53, 4258–4263 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Pecharki, D., Petersen, F. C. & Scheie, A. A. LuxS and expression of virulence factors in Streptococcus intermedius. Oral Microbiol. Immunol. 23, 79–83 (2008).
  Article CAS PubMed Google Scholar
• Semmelhack, M. F., Campagna, S. R., Federle, M. J. & Bassler, B. L. An expeditious synthesis of DPD and boron binding studies. Org. Lett. 7, 569–572 (2005).
  Article CAS PubMed Google Scholar
• Frias, J., Olle, E. & Alsina, M. Periodontal pathogens produce quorum sensing signal molecules. Infect. Immun. 69, 3431–3434 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Li, J. et al. Identification of early microbial colonizers in human dental biofilm. J. Appl. Microbiol. 97, 1311–1318 (2004).
  Article CAS Google Scholar
• 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. 57, 3194–3203 (1989).
  CAS PubMed PubMed Central Google Scholar
• Moore, W. E. & Moore, L. V. The bacteria of periodontal diseases. Periodontol. 2000 5, 66–77 (1994).
  Article CAS PubMed Google Scholar
• Taga, M. E., Miller, S. T. & Bassler, B. L. Lsr-mediated transport and processing of AI-2 in Salmonella typhimurium. Mol. Microbiol. 50, 1411–1427 (2003).
  Article CAS PubMed Google Scholar
• Shao, H., James, D., Lamont, R. J. & Demuth, D. R. Differential interaction of Aggregatibacter (Actinobacillus) actinomycetemcomitans LsrB and RbsB proteins with autoinducer 2. J. Bacteriol. 189, 5559–5565 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Shao, H., Lamont, R. J. & Demuth, D. R. Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect. Immun. 75, 4211–4218 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Roberts, A. P. et al. Transfer of TN916-like elements in microcosm dental plaques. Antimicrob. Agents Chemother. 45, 2943–2946 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Warburton, P. J., Palmer, R. M., Munson, M. A. & Wade, W. G. Demonstration of in vivo transfer of doxycycline resistance mediated by a novel transposon. J. Antimicrob. Chemother. 60, 973–980 (2007).
  Article CAS PubMed Google Scholar
• Rice, L. B. Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob. Agents Chemother. 42, 1871–1877 (1998).
  Article CAS PubMed PubMed Central Google Scholar
• Mira, A. in Molecular Oral Microbiology, (ed Rogers, A. H.) 65–85 (Caister, Norfolk, UK, 2008).
  Google Scholar
• Naito, M. et al. Determination of the genome sequence of Porphyromonas gingivalis strain ATCC 33277 and genomic comparison with strain W83 revealed extensive genome rearrangements in P. gingivalis. DNA Res. 15, 215–225 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Koehler, A. et al. Multilocus sequence analysis of Porphyromonas gingivalis indicates frequent recombination. Microbiology 149, 2407–2415 (2003).
  Article CAS PubMed Google Scholar
• Tribble, G. D., Lamont, G. J., Progulske-Fox, A. & Lamont, R. J. Conjugal transfer of chromosomal DNA contributes to genetic variation in the oral pathogen Porphyromonas gingivalis. J. Bacteriol. 189, 6382–6388 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Wang, B. Y., Chi, B. & Kuramitsu, H. K. Genetic exchange between Treponema denticola and Streptococcus gordonii in biofilms. Oral Microbiol. Immunol. 17, 108–112 (2002).
  Article CAS PubMed Google Scholar
• Li, Y. H., Lau, P. C., Lee, J. H., Ellen, R. P. & Cvitkovitch, D. G. Natural genetic transformation of Streptococcus mutans growing in biofilms. J. Bacteriol. 183, 897–908 (2001).
  Article CAS PubMed PubMed Central Google Scholar
• Petersen, F. C., Tao, L. & Scheie, A. A. DNA binding-uptake system: a link between cell-to-cell communication and biofilm formation. J. Bacteriol. 187, 4392–4400 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Tamura, S. et al. Inhibiting effects of Streptococcus salivarius on competence-stimulating peptide-dependent biofilm formation by Streptococcus mutans. Oral Microbiol. Immunol. 24, 152–161 (2009).
  Article CAS PubMed Google Scholar
• Wang, B. Y. & Kuramitsu, H. K. Interactions between oral bacteria: inhibition of Streptococcus mutans bacteriocin production by Streptococcus gordonii. Appl. Environ. Microbiol. 71, 354–362 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Kreth, J., Merritt, J., Shi, W. & Qi, F. Co-ordinated bacteriocin production and competence development: a possible mechanism for taking up DNA from neighbouring species. Mol. Microbiol. 57, 392–404 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Perry, J. A., Jones, M. B., Peterson, S. N., Cvitkovitch, D. G. & Levesque, C. M. Peptide alarmone signalling triggers an auto-active bacteriocin necessary for genetic competence. Mol. Microbiol. 72, 905–917 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Steinberger, R. E. & Holden, P. A. Extracellular DNA in single- and multiple-species unsaturated biofilms. Appl. Environ. Microbiol. 71, 5404–5410 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Tetz, G. V., Artemenko, N. K. & Tetz, V. V. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob. Agents Chemother. 53, 1204–1209 (2009).
  Article CAS PubMed Google Scholar
• Mulcahy, H., Charron-Mazenod, L. & Lewenza, S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Agnelli, A. et al. Distribution of microbial communities in a forest soil profile investigated by microbial biomass, soil respiration and DGGE of total and extracellular DNA. Soil Biol. Biochem. 36, 859–868 (2004).
  Article CAS Google Scholar
• Gao, Z., Tseng, C.-H., Pei, Z. & Blaser, M. J. Molecular analysis of human forearm superficial skin bacterial biota. Proc. Natl Acad. Sci. USA 104, 2927–2932 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Kroes, I., Lepp, P. W. & Relman, D. A. Bacterial diversity within the human subgingival crevice. Proc. Natl Acad. Sci. USA 96, 14547–14552 (1999).
  Article CAS PubMed PubMed Central Google Scholar
• Marcy, Y. et al. Dissecting biological “dark matter” with single-cell genetic analysis of rare and uncultivated TM7 microbes from the human mouth. Proc. Natl Acad. Sci. 104, 11889–11894 (2007).
  Article CAS PubMed PubMed Central Google Scholar
• Kaeberlein, T., Lewis, K. & Epstein, S. S. Isolating “uncultivable” microorganisms in pure culture in a simulated natural environment. Science 296, 1127–1129 (2002).
  Article CAS PubMed Google Scholar
• Branda, S. S. et al. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J. Bacteriol. 186, 3970–3979 (2004).
  Article CAS PubMed PubMed Central Google Scholar
• Kearns, D. B. & Losick, R. Cell population heterogeneity during growth of Bacillus subtilis. Genes Dev. 19, 3083–3094 (2005).
  Article CAS PubMed PubMed Central Google Scholar
• Blevins, J. S., Beenken, K. E., Elasri, M. O., Hurlburt, B. K. & Smeltzer, M. S. Strain-dependent differences in the regulatory roles of sarA and agr in Staphylococcus aureus. Infect. Immun. 70, 470–480 (2002).
  Article CAS PubMed PubMed Central Google Scholar
• Fine, D. H. et al. Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 145, 1335–1347 (1999).
  Article CAS PubMed Google Scholar
• Saito, A. et al. Fusobacterium nucleatum enhances invasion of human gingival epithelial and aortic endothelial cells by Porphyromonas gingivalis. FEMS Immunol. Med. Microbiol. 54, 349–355 (2008).
  Article CAS PubMed Google Scholar
• Takahashi, N. & Nyvad, B. Caries ecology revisited: microbial dynamics and the caries process. Caries Res. 42, 409–418 (2008).
  Article CAS PubMed Google Scholar
• Pereira, C. S., McAuley, J. R., Taga, M. E., Xavier, K. B. & Miller, S. T. Sinorhizobium meliloti, a bacterium lacking the autoinducer-2 (AI-2) synthase, responds to AI-2 supplied by other bacteria. Mol. Microbiol. 70, 1223–1235 (2008).
  Article CAS PubMed PubMed Central Google Scholar
• Takenaka, S., Pitts, B., Trivedi, H. M. & Stewart, P. S. Diffusion of macromolecules in model oral biofilms. Appl. Environ. Microbiol. 75, 1750–1753 (2009).
  Article CAS PubMed PubMed Central Google Scholar
• Kuboniwa, M. et al. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol. Microbiol. 60, 121–139 (2006).
  Article CAS PubMed Google Scholar
• Kolenbrander, P. E. et al. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66, 486–505 (2002).
  Article CAS PubMed PubMed Central Google Scholar