Oral multispecies biofilm development and the key role of cell-cell distance

Nature Reviews Microbiology

Volumn 8, Issue 7, 2010, Pages 471-480

  Kolenbrander, Paul E ^a   Palmer, Robert J ^a   Periasamy, Saravanan ^a   Jakubovics, Nicholas S ^b  

^a NATIONAL INSTITUTE OF DENTAL AND CRANIOFACIAL RESEARCH   (United States)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL COLONIZATION; BACTERIAL GROWTH; BACTERIUM ADHERENCE; BACTERIUM CULTURE; BACTERIUM IDENTIFICATION; BIOFILM; BIOGEOGRAPHY; CELL INTERACTION; DNA TRANSFER; FUSOBACTERIUM; GENE EXPRESSION; MOUTH CAVITY; NONHUMAN; OROPHARYNX; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; STREPTOCOCCUS;

BIOFILMS; HUMANS; METAGENOME; MOUTH; PERIODONTAL DISEASES; SALIVA;

BACTERIA (MICROORGANISMS);

EID: 77953620116     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro2381     Document Type: Review

References (106)

1. Achtman, M. & Wagner, M. Microbial diversity and the genetic nature of microbial species. Nature Rev. Microbiol. 6, 431-440 (2008).
2. 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).
3. Lozupone, C. A. & Knight, R. Species divergence and the measurement of microbial diversity. FEMS Microbiol Rev. 32, 557-578 (2008).
4. 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).
5. Zaura, E., Keijser, B. J., Huse, S. M. & Crielaard, W. Defining the healthy "core microbiome" of oral microbial communities. BMC Microbiol. 9, 259 (2009).
6. 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).
7. 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).
8. 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). (Pubitemid 32763615)
9. Kolenbrander, P. E. & London, J. Adhere today, here tomorrow: oral bacterial adherence. J. Bacteriol. 175, 3247-3252 (1993).
10. 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).
11. 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).
12. 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).
13. Diaz, P. I. et al. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72, 2837-2848 (2006).
14. 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. 11 5, 459-467 (2007).
15. 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).
16. Dige, I., Raarup, M. K., Nyengaard, J. R., Kilian, M. & Nyvad, B. Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155, 2116-2126 (2009).
17. 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).
18. 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).
19. 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).
20. 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).
21. 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).
22. 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).
23. 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).
24. 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).
25. 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).
26. 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).
27. Periasamy, S., Chalmers, N. I., Du-Thumm, L. & Kolenbrander, P. E. Fusobacterium nucleatum ATCC 10953 requires Actinomyces naeslundii ATC C 43146 for growth on saliva in a three-species community that includes Streptococcus oralis 34. Appl. Environ. Microbiol. 75, 3250-3257 (2009).
28. 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).
29. 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).
30. Rickard, A. H. et al. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60, 1446-1456 (2006).
31. 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).
32. 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).
33. 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).
34. Buckley, M. R. Microbial communities: from life apart to life together. American Academy of Microbiology [online] http://academy.asm.org/index.php? option=com-content&view=article&id=226:microbial-communities-from-life- apart-to-life-together-2002&catid=40:browse-all&Itemid=79 (2002).
35. 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).
36. 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).
37. Keller, L. & Surette, M. G. Communication in bacteria: an ecological and evolutionary perspective. Nature Rev. Microbiol. 4, 249-258 (2006).
38. Redfield, R. J. Is quorum sensing a side effect of diffusion sensing? Trends Microbiol. 10, 365-370 (2002).
39. 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).
40. 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).
41. Handfield, M. et al. Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell. Microbiol. 7, 811-823 (2005).
42. Hasegawa, Y. et al. Gingival epithelial cell transcriptional responses to commensal and opportunistic oral microbial species. Infect. Immun. 75, 2540-2547 (2007).
43. 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).
44. Wickstrom, C. & Svensater, G. Salivary gel-forming mucin MUC5B-a nutrient for dental plaque bacteria. Oral Microbiol. Immunol. 23, 177-182 (2008).
45. Dawes, C. What is the critical pH and why does a tooth dissolve in acid? J. Can. Dent. Assoc. 69, 722-724 (2003).
46. de Soet, J. J., Nyvad, B. & Kilian, M. Strain-related acid production by oral streptococci. Caries Res. 34, 486-490 (2000).
47. Burne, R. A. & Marquis, R. E. Alkali production by oral bacteria and protection against dental caries. FEMS Microbiol. Lett. 193, 1-6 (2000).
48. Marsh, P. D. Are dental diseases examples of ecological catastrophes? Microbiology 149, 279-294 (2003).
49. Becker, M. R. et al. Molecular analysis of bacterial species associated with childhood caries. J. Clin. Microbiol. 40, 1001-1009 (2002).
50. Lo, E. C., Schwarz, E. & Wong, M. C. Arresting dentine caries in Chinese preschool children. Int. J. Paediatr. Dent. 8, 253-260 (1998).
51. 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).
52. Socransky, S. S., Smith, C. & Haffajee, A. D. Subgingival microbial profiles in refractory periodontal disease. J. Clin. Periodontol. 29, 260-268 (2002).
53. 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).
54. 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).
55. Merritt, J., Niu, G., Okinaga, T. & Qi, F. Autoaggregation response of Fusobacterium nucleatum. Appl. Environ. Microbiol. 75, 7725-7733 (2009).
56. 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).
57. 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).
58. Kuboniwa, M. et al. Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol. 9, 98 (2009).
59. Simionato, M. R. et al. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74, 6419-6428 (2006).
60. 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).
61. Johnson, B. P. et al. Interspecies signaling between Veillonella atypica and Streptococcus gordonii requires the transcription factor CcpA. J. Bacteriol. 191, 5563-5565 (2009).
62. Bamford, C. V. et al. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 77, 3696-3704 (2009).
63. Samaranayake, L. P., Keung Leung, W. & Jin, L. Oral mucosal fungal infections. Periodontol. 2000 49, 39-59 (2009).
64. 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).
65. 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).
66. Pecharki, D., Petersen, F. C. & Scheie, A. A. LuxS and expression of virulence factors in Streptococcus intermedius. Oral Microbiol. Immunol. 23, 79-83 (2008).
67. 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).
68. Frias, J., Olle, E. & Alsina, M. Periodontal pathogens produce quorum sensing signal molecules. Infect. Immun. 69, 3431-3434 (2001).
69. Li, J. et al. Identification of early microbial colonizers in human dental biofilm. J. Appl. Microbiol. 97, 1311-1318 (2004).
70. 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).
71. Moore, W. E. & Moore, L. V. The bacteria of periodontal diseases. Periodontol. 2000 5, 66-77 (1994).
72. 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).
73. 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).
74. 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).
75. Roberts, A. P. et al. Transfer of TN916-like elements in microcosm dental plaques. Antimicrob. Agents Chemother. 45, 2943-2946 (2001).
76. 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).
77. Rice, L. B. Tn916 family conjugative transposons and dissemination of antimicrobial resistance determinants. Antimicrob. Agents Chemother. 42, 1871-1877 (1998)
78. Mira, A. in Molecular Oral Microbiology, (ed Rogers, A. H.) 65-85 (Caister, Norfolk, UK, 2008).
79. 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).
80. Koehler, A. et al. Multilocus sequence analysis of Porphyromonas gingivalis indicates frequent recombination. Microbiology 149, 2407-2415 (2003).
81. 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).
82. 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).
83. 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).
84. 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).
85. 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).
86. 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).
87. 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).
88. 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).
89. Steinberger, R. E. & Holden, P. A. Extracellular DNA in single-and multiple-species unsaturated biofilms. Appl. Environ. Microbiol. 71, 5404-5410 (2005).
90. Tetz, G. V., Artemenko, N. K. & Tetz, V. V. Effect of DNase and antibiotics on biofilm characteristics. Antimicrob. Agents Chemother. 53, 1204-1209 (2009).
91. Mulcahy, H., Charron-Mazenod, L. & Lewenza, S. Extracellular DNA chelates cations and induces antibiotic resistance in Pseudomonas aeruginosa biofilms. PLoS Pathog. 4, e1000213 (2008).
92. 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).
93. 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).
94. Kroes, I., Lepp, P. W. & Relman, D. A. Bacterial diversity within the human subgingival crevice. Proc. Natl Acad. Sci. USA 96, 14547-14552 (1999).
95. 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).
96. Kaeberlein, T., Lewis, K. & Epstein, S. S. Isolating "uncultivable" microorganisms in pure culture in a simulated natural environment. Science 296, 1127-1129 (2002).
97. Branda, S. S. et al. Genes involved in formation of structured multicellular communities by Bacillus subtilis. J. Bacteriol. 186, 3970-3979 (2004).
98. Kearns, D. B. & Losick, R. Cell population heterogeneity during growth of Bacillus subtilis. Genes D e v. 19, 3083-3094 (2005).
99. 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).
100. Fine, D. H. et al. Phenotypic variation in Actinobacillus actinomycetemcomitans during laboratory growth: implications for virulence. Microbiology 145, 1335-1347 (1999).
101. 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).
102. Takahashi, N. & Nyvad, B. Caries ecology revisited: microbial dynamics and the caries process. Caries Res. 42, 409-418 (2008).
103. 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).
104. Takenaka, S., Pitts, B., Trivedi, H. M. & Stewart, P. S. Diffusion of macromolecules in model oral biofilms. Appl. Environ. Microbiol. 75, 1750-1753 (2009).
105. 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).
106. Kolenbrander, P. E. et al. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66, 486-505 (2002).