1887

Chapter 1 : Interspecies Interactions Promote Multispecies Communities

MyBook is a cheap paperback edition of the original book and will be sold at uniform, low price.

Ebook: Choose a downloadable PDF or ePub file. Chapter is a downloadable PDF file. File must be downloaded within 48 hours of purchase

Buy this Chapter
Digital (?) $15.00

Preview this chapter:
Zoom in
Zoomout

Interspecies Interactions Promote Multispecies Communities, Page 1 of 2

| /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap01-1.gif /docserver/preview/fulltext/10.1128/9781555817107/9781555815035_Chap01-2.gif

Abstract:

Multispecies communities, not a collection of single-species colonies, compose human oral biofilms. The human oral microbiome is the most intensely studied and, perhaps, the best-characterized ecosystem in humans, but the organization of these species into multispecies communities at any point in time remains poorly understood. Genomic inquiry of community members will enable a fuller vision of each member’s metabolic contribution to the community. A central contributor to colonization of oral bacteria in biofilms is the universal ability of these species to attach to a surface: to teeth or to epithelial cell surfaces or to the bacterial surface of an already attached cell. Cells suspended in saliva are unable to multiply within a typical between-swallows interval due to the rapid salivary flow. Thus, adherence is essential before multispecies communities can develop and colonize the surface. Following coadherence and coaggregation, attached cells grow, as evidenced by incorporation of radiolabeled nucleosides and by cell division planes observed in the biofilms of intraoral mounted pieces of enamel or glass. Evidence-based two-species and three-species biofilms contribute in understanding species succession leading to a crossroad between health and disease in dental plaque biofilms. Virulence mechanisms exhibited by red complex periodontal pathogens are discussed in an inspired review of the interplay between pathogenic and commensal bacteria in disrupting host homeostasis. It is recognized that multispecies communities respond differently than pure cultures to antimicrobials.

Citation: Kolenbrander P, Periasamy S. 2011. Interspecies Interactions Promote Multispecies Communities, p 3-19. In Kolenbrander P (ed), Oral Microbial Communities. ASM Press, Washington, DC. doi: 10.1128/9781555817107.ch1

Key Concept Ranking

Streptococcus oralis
0.70672363
Streptococcus sanguinis
0.70672363
Streptococcus oralis
0.70672363
Streptococcus sanguinis
0.70672363
Streptococcus oralis
0.70672363
Streptococcus sanguinis
0.70672363
Streptococcus oralis
0.70672363
0.70672363
Highlighted Text: Show | Hide
Loading full text...

Full text loading...

References

/content/book/10.1128/9781555817107.ch01
1. Aas, J. A.,, B. J. Paster,, L. N. Stokes,, I. Olsen, and, F. E. Dewhirst. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43:57215732.
2. Andrian, E.,, D. Grenier, and, M. Rouabhia. 2004. In vitro models of tissue penetration and destruction by Porphyromonas gingivalis. Infect. Immun. 72:46894698.
3. Bachrach, G.,, H. Altman,, P. E. Kolenbrander,, N. I. Chalmers,, M. Gabai-Gutner,, A. Mor,, M. Friedman, and, D. Steinberg. 2008. Resistance of Porphyromonas gingivalis ATCC 33277 to direct killing by antimicrobial peptides is protease independent. Antimicrob. Agents Che-mother. 52:638642.
4. Bamford, C. V.,, A. d’Mello,, A. H. Nobbs,, L. C. Dutton,, M. M. Vickerman, and, H. F. Jenkinson. 2009. Streptococcus gordonii modulates Candida albicans biofilm formation through intergeneric communication. Infect. Immun. 77:36963704.
5. Becker, M. R.,, B. J. Paster,, E. J. Leys,, M. L. Moeschberger,, S. G. Kenyon,, J. L. Galvin,, S. K. Boches,, F. E. Dewhirst, and, A. L. Griffen. 2002. Molecular analysis of bacterial species associated with childhood caries. J. Clin. Microbiol. 40:10011009.
6. Beighton, D. 2005. The complex oral microflora of high-risk individuals and groups and its role in the caries process. Community Dent. Oral Epidemiol. 33:248255.
7. Bek-Thomsen, M.,, H. Tettelin,, I. Hance,, K. E. Nelson, and, M. Kilian. 2008. Population diversity and dynamics of Streptococcus mitis, Streptococcus oralis, and Streptococcus infantis in the upper respiratory tracts of adults, determined by a non-culture strategy. Infect. Immun. 76:18891896.
8. Bian, X. L.,, H. T. Wang,, Y. Ning,, S. Y. Lee, and, J. C. Fenno. 2005. Mutagenesis of a novel gene in the prcA-prtP protease locus affects expression of Treponema denticola membrane complexes. Infect. Immun. 73:12521255.
9. Bik, E. M.,, C. D. Long,, G. C. Armitage,, P. Loomer,, J. Emerson,, E. F. Mongodin,, K. E. Nelson,, S. R. Gill,, C. M. Fraser-Liggett, and, D. A. Relman. 2010. Bacterial diversity in the oral cavity of 10 healthy individuals. ISME J. 4:962974.
10. Bloomquist, C. G.,, B. E. Reilly, and, W. F. Liljemark. 1996. Adherence, accumulation, and cell division of a natural adherent bacterial population. J. Bacteriol. 178:11721177.
11. Bos, R.,, H. C. van der Mei, and, H. J. Busscher. 1996. Co-adhesion of oral microbial pairs under flow in the presence of saliva and lactose. J. Dent. Res. 75:809815.
12. Brady, L. J.,, S. E. Maddocks,, M. R. Larson,, N. Forsgren,, K. Persson,, C. C. Deivanayagam, and, H. F. Jenkinson. 2010. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Mol. Microbiol. 77:276286.
13. Brogden, K. A.,, J. M. Guthmiller,, M. Salzet, and, M. Zasloff. 2005. The nervous system and innate immunity: the neuropeptide connection. Nat. Immunol. 6:558564.
14. Busscher, H. J.,, W. Norde, and, H. C. van der Mei. 2008. Specific molecular recognition and nonspecific contributions to bacterial interaction forces. Appl. Environ. Microbiol. 74:25592564.
15. Carlisle, M. D.,, R. N. Srikantha, and, K. A. Brogden. 2009. Degradation of human alpha-and beta-defensins by culture supernatants of Porphyromonas gingivalis strain 381. J. Innate Immun. 1:118122.
16. Chalmers, N. I.,, R. J. Palmer, Jr.,, J. O. Cisar, and, P. E. Kolenbrander. 2008. Characterization of a Streptococcus sp.-Veillonella sp. community micromanipulated from dental plaque. J. Bacteriol. 190:81458154.
17. Chawla, A.,, T. Hirano,, B. W. Bainbridge,, D. R. Demuth,, H. Xie, and, R. J. Lamont. 2010. Community signalling between Streptococcus gordonii and Porphyromonas gingivalis is controlled by the transcriptional regulator CdhR. Mol. Microbiol. 78:15101522.
18. Crowley, P. J.,, W. Fischlschweiger,, S. E. Coleman, and, A. S. Bleiweis. 1987. Intergeneric bacterial coaggregations involving mutans streptococci and oral actinomyces. Infect. Immun. 55:26952700.
19. Daep, C. A.,, D. M. James,, R. J. Lamont, and, D. R. Demuth. 2006. Structural characterization of peptide-mediated inhibition of Porphyromonas gingivalis biofilm formation. Infect. Immun. 74:57565762.
20. Daep, C. A.,, R. J. Lamont, and, D. R. Demuth. 2008. Interaction of Porphyromonas gingivalis with oral streptococci requires a motif that resembles the eukaryotic nuclear receptor box protein-protein interaction domain. Infect. Immun. 76:32733280.
21. Darveau, R. P. 2010. Periodontitis: a polymicrobial disruption of host homeostasis. Nat. Rev. Microbiol. 8:481490.
22. Darveau, R. P.,, C. M. Belton,, R. A. Reife, and, R. J. Lamont. 1998. Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect. Immun. 66:16601665.
23. Devine, D. A.,, P. D. Marsh,, R. S. Percival,, M. Rangarajan, and, M. A. Curtis. 1999. Modulation of antibacterial peptide activity by products of Porphyromonas gingivalis and Prevotella spp. Microbiology 145:965971.
24. Dewhirst, F. E.,, T. Chen,, J. Izard,, B. J. Paster,, A. C. Tanner,, W. H. Yu,, A. Lakshmanan, and, W. G. Wade. 2010. The human oral microbiome. J. Bacteriol. 192:50025017.
25. Diaz, P. I.,, N. I. Chalmers,, A. H. Rickard,, C. Kong,, C. L. Milburn,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2006. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl. Environ. Microbiol. 72:28372848.
26. Diaz, P. I.,, N. Slakeski,, E. C. Reynolds,, R. Morona,, A. H. Rogers, and, P. E. Kolenbrander. 2006. Role of oxyR in the oral anaerobe Porphyromonas gingivalis. J. Bacteriol. 188:24542462.
27. Dige, I.,, H. Nilsson,, M. Kilian, and, B. Nyvad. 2007. 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. 115:459467.
28. Dige, I.,, M. K. Raarup,, J. R. Nyengaard,, M. Kilian, and, B. Nyvad. 2009. Actinomyces naeslundii in initial dental biofilm formation. Microbiology 155:21162126.
29. Dongari-Bagtzoglou, A.,, and H. Kashleva. 2006. Development of a highly reproducible three-dimensional organotypic model of the oral mucosa. Nat. Protoc. 1:20122018.
30. Dongari-Bagtzoglou, A.,, H. Kashleva,, P. Dwivedi,, P. Diaz, and, J. Vasilakos. 2009. Characterization of mucosal Candida albicans biofilms. PLoS One 4:e7967.
31. Dorn, B. R.,, K. L. Leung, and, A. Progulske-Fox. 1998. Invasion of human oral epithelial cells by Prevotella intermedia. Infect. Immun. 66:60546057.
32. Edwards, A. M.,, T. J. Grossman, and, J. D. Rudney. 2007. Association of a high-molecular weight arginine-binding protein of Fusobacterium nucleatum ATCC 10953 with adhesion to secretory immunoglobulin A and coaggregation with Streptococcus cristatus. Oral Microbiol. Immunol. 22:217224.
33. Egland, P. G.,, L. D. Du, and, P. E. Kolenbrander. 2001. Identification of independent Streptococcus gordonii SspA and SspB functions in coaggregation with Actinomyces naeslundii. Infect. Immun. 69:75127516.
34. Egland, P. G.,, R. J. Palmer, Jr., and, P. E. Kolenbrander. 2004. Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc. Natl. Acad. Sci. USA 101:1691716922.
35. Exterkate, R. A.,, W. Crielaard, and, J. M. Ten Cate. 2010. Different response to amine fluoride by Streptococcus mutans and polymicrobial biofilms in a novel high-throughput active attachment model. Caries Res. 44:372379.
36. Fong, K. P.,, W. O. Chung,, R. J. Lamont, and, D. R. Demuth. 2001. Intra-and interspecies regulation of gene expression by Actinobacillus actinomycetemcomitans LuxS. Infect. Immun. 69:76257634.
37. Gibbons, R. J.,, and M. Nygaard. 1970. Interbacterial aggregation of plaque bacteria. Arch. Oral Biol. 15:13971400.
38. Godovikova, V.,, H. T. Wang,, M. P. Goetting-Minesky,, Y. Ning,, R. F. Capone,, C. K. Slater, and, J. C. Fenno. 2010. Treponema denticola PrcB is required for expression and activity of the PrcA-PrtP (dentilisin) complex. J. Bacteriol. 192:33373344.
39. Gupta, S.,, S. K. Ghosh,, M. E. Scott,, B. Bainbridge,, B. Jiang,, R. J. Lamont,, T. S. McCormick, and, A. Weinberg. 2010. Fusobacterium nucleatum-associated beta-defensin inducer (FAD-I): identification, isolation, and functional evaluation. J. Biol. Chem. 285:3652336531.
40. Gursoy, U. K.,, M. Pollanen,, E. Kononen, and, V. J. Uitto. 2010. Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J. Periodontol. 81:10841091.
41. Gutner, M.,, S. Chaushu,, D. Balter, and, G. Bachrach. 2009. Saliva enables the antimicrobial activity of LL-37 in the presence of proteases of Porphyromonas gingivalis. Infect. Immun. 77:55585563.
42. Haake, S. K.,, S. C. Yoder,, G. Attarian, and, K. Podkaminer. 2000. Native plasmids of Fusobacterium nucleatum: characterization and use in development of genetic systems. J. Bacteriol. 182:11761180.
43. Han, Y. W.,, A. Ikegami,, P. Chung,, L. Zhang, and, C. X. Deng. 2007. Sonoporation is an efficient tool for intracellular fluorescent dextran delivery and one-step double-crossover mutant construction in Fusobacterium nucleatum. Appl. Environ. Microbiol. 73:36773683.
44. Han, Y. W.,, W. Shi,, G. T. Huang,, S. Kinder Haake,, N. H. Park,, H. Kuramitsu, and, R. J. Genco. 2000. Interactions between periodontal bacteria and human oral epithelial cells: Fusobacterium nucleatum adheres to and invades epithelial cells. Infect. Immun. 68:31403146.
45. Hasegawa, Y.,, J. J. Mans,, S. Mao,, M. C. Lopez,, H. V. Baker,, M. Handfield, and, R. J. Lamont. 2007. Gingival epithelial cell transcriptional responses to commensal and opportunistic oral microbial species. Infect. Immun. 75:25402547.
46. Hashimoto, M.,, S. Ogawa,, Y. Asai,, Y. Takai, and, T. Ogawa. 2003. Binding of Porphyromonas gingivalis fimbriae to Treponema denticola dentilisin. FEMS Microbiol. Lett. 226:267271.
47. Honma, K.,, E. Mishima,, S. Inagaki, and, A. Sharma. 2009. The OxyR homologue in Tannerella forsythia regulates expression of oxidative stress responses and biofilm formation. Microbiology 155:19121922.
48. Ikegami, A.,, P. Chung, and, Y. W. Han. 2009. Complementation of the fadA mutation in Fusobacterium nucleatum demonstrates that the surface-exposed adhesin promotes cellular invasion and placental colonization. Infect. Immun. 77:30753079.
49. Inagaki, S.,, S. Onishi,, H. K. Kuramitsu, and, A. Sharma. 2006. Porphyromonas gingivalis vesicles enhance attachment, and the leucine-rich repeat BspA protein is required for invasion of epithelial cells by “Tannerella forsythia.” Infect. Immun. 74:50235028.
50. Iyer, D.,, C. Anaya-Bergman,, K. Jones,, S. Yanamandra,, D. Sengupta,, H. Miyazaki, and, J. P. Lewis. 2010. AdpC is a Prevotella intermedia 17 leucine-rich repeat internalin-like protein. Infect. Immun. 78:23852396.
51. Jakubovics, N. S.,, S. R. Gill,, S. E. Iobst,, M. M. Vickerman, and, P. E. Kolenbrander. 2008. Regulation of gene expression in a mixedgenus community: stabilized arginine biosynthesis in Streptococcus gordonii by coaggregation with Actinomyces naeslundii. J. Bacteriol. 190:36463657.
52. Jakubovics, N. S.,, N. Stromberg,, C. J. van Dolleweerd,, C. G. Kelly, and, H. F. Jenkinson. 2005. Differential binding specificities of oral streptococcal antigen I/II family adhesins for human or bacterial ligands. Mol. Microbiol. 55:15911605.
53. Johnson, B. P.,, B. J. Jensen,, E. M. Ransom,, K. A. Heinemann,, K. M. Vannatta,, K. A. Egland, and, P. G. Egland. 2009. Interspecies signaling between Veillonella atypica and Streptococcus gordonii requires the transcription factor CcpA. J. Bacteriol. 191:55635565.
54. Kanasi, E.,, F. E. Dewhirst,, N. I. Chalmers,, R. Kent, Jr.,, A. Moore,, C. V. Hughes,, N. Pradhan,, C. Y. Loo, and, A. C. Tanner. 2010. Clonal analysis of the microbiota of severe early childhood caries. Caries Res. 44:485497.
55. Kapatral, V.,, I. Anderson,, N. Ivanova,, G. Reznik,, T. Los,, A. Lykidis,, A. Bhattacharyya,, A. Bartman,, W. Gardner,, G. Grechkin,, L. Zhu,, O. Vasieva,, L. Chu,, Y. Kogan,, O. Chaga,, E. Goltsman,, A. Bernal,, N. Larsen,, M. D’Souza,, T. Walunas,, G. Pusch,, R. Haselkorn,, M. Fonstein,, N. Kyrpides, and, R. Overbeek. 2002. Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 184:20052018.
56. Kapatral, V.,, N. Ivanova,, I. Anderson,, G. Reznik,, A. Bhattacharyya,, W. L. Gardner,, N. Mikhailova,, A. Lapidus,, N. Larsen,, M. D’Souza,, T. Walunas,, R. Haselkorn,, R. Overbeek, and, N. Kyrpides. 2003. Genome analysis of F. nucleatum sub spp vincentii and its comparison with the genome of F. nucleatum ATCC 25586. Genome Res. 13:11801189.
57. Kaplan, C. W.,, R. Lux,, S. K. Haake, and, W. Shi. 2009. The Fusobacterium nucleatum outer membrane protein RadD is an arginineinhibitable adhesin required for inter-species adherence and the structured architecture of multispecies biofilm. Mol. Microbiol. 71:3547.
58. Kaplan, C. W.,, R. Lux,, T. Huynh,, A. Jewett,, W. Shi, and, S. K. Haake. 2005. Fusobacterium nucleatum apoptosis-inducing outer membrane protein. J. Dent. Res. 84:700704.
59. Kaplan, C. W.,, X. Ma,, A. Paranjpe,, A. Jewett,, R. Lux,, S. Kinder-Haake, and, W. Shi. 2010. Fusobacterium nucleatum outer membrane proteins, Fap2 and RadD, induce cell death in human lymphocytes. Infect. Immun. 78:47734778.
60. Karpathy, S. E.,, X. Qin,, J. Gioia,, H. Jiang,, Y. Liu,, J. F. Petrosino,, S. Yerrapragada,, G. E. Fox,, S. K. Haake,, G. M. Weinstock, and, S. K. Highlander. 2007. Genome sequence of Fusobacterium nucleatum subspecies polymorphum—a genetically tractable fusobacterium. PLoS One 2:e659.
61. Kawamura, Y.,, X. G. Hou,, F. Sultana,, H. Miura, and, T. Ezaki. 1995. Determination of 16S rRNA sequences of Streptococcus mitis and Streptococcus gordonii and phylogenetic relationships among members of the genus Streptococcus. Int. J. Syst. Bacteriol. 45:406408.
62. Kilian, M.,, M. J. Larsen,, O. Fejerskov, and, A. Thylstrup. 1979. Effects of fluoride on the initial colonization of teeth in vivo. Caries Res. 13:319329.
63. Kolenbrander, P. E. 1988. Intergeneric coaggregation among human oral bacteria and ecology of dental plaque. Annu. Rev. Microbiol. 42:627656.
64. Kolenbrander, P. E. 2000. Oral microbial communities: biofilms, interactions, and genetic systems. Annu. Rev. Microbiol. 54:413437.
65. Kolenbrander, P. E.,, R. N. Andersen,, D. S. Blehert,, P. G. Egland,, J. S. Foster, and, R. J. Palmer, Jr. 2002. Communication among oral bacteria. Microbiol. Mol. Biol. Rev. 66:486505.
66. Kolenbrander, P. E.,, R. N. Andersen, and, L. V. Moore. 1989. Coaggregation of Fusobacterium nucleatum, Selenomonas flueggei, Selenomonas infelix, Selenomonas noxia, and Selenomonas sputigena with strains from 11 genera of oral bacteria. Infect. Immun. 57:31943203.
67. Kolenbrander, P. E.,, R. N. Andersen, and, L. V. Moore. 1990. Intrageneric coaggregation among strains of human oral bacteria: potential role in primary colonization of the tooth surface. Appl. Environ. Microbiol. 56:38903894.
68. Kolenbrander, P. E.,, N. Ganeshkumar,, F. J. Cassels, and, C. V. Hughes. 1993. Coaggregation: specific adherence among human oral plaque bacteria. FASEB J. 7:406413.
69. Kolenbrander, P. E.,, N. S. Jakubovics,, N. I. Chalmers, and, G. Bachrach. 2007. Coaggregation and distance-critical communication, p. 89–100. In K. A. Brogden,, F. C. Minion,, N. Cornick,, T. B. Stanton,, Q. Zhang,, L. K. Nolan, and, M. J. Wannemuehler (ed.), Virulence Mechanisms of Bacterial Pathogens, 4th ed. ASM Press, Washington, DC.
70. Kolenbrander, P. E.,, and J. London. 1993. Adhere today, here tomorrow: oral bacterial adherence. J. Bacteriol. 175:32473252.
71. Kolenbrander, P. E.,, R. J. Palmer, Jr.,, S. Periasamy, and, N. S. Jakubovics. 2010. Oral multispecies biofilm development and the key role of cell-cell distance. Nat. Rev. Microbiol. 8:471480.
72. Kolenbrander, P. E.,, R. J. Palmer, Jr.,, A. H. Rickard,, N. S. Jakubovics,, N. I. Chalmers, and, P. I. Diaz. 2006. Bacterial interactions and successions during plaque development. Periodontol. 2000 42:4779.
73. Koo, H.,, J. Xiao,, M. I. Klein, and, J. G. Jeon. 2010. Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J. Bacteriol. 192:30243032.
74. Kreth, J.,, J. Merritt,, W. Shi, and, F. Qi. 2005. Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J. Bacteriol. 187:71937203.
75. Krisanaprakornkit, S.,, J. R. Kimball,, A. Weinberg,, R. P. Darveau,, B. W. Bainbridge, and, B. A. Dale. 2000. Inducible expression of human beta-defensin 2 by Fusobacterium nucleatum in oral epithelial cells: multiple signaling pathways and role of commensal bacteria in innate immunity and the epithelial barrier. Infect. Immun. 68:29072915.
76. Kuboniwa, M.,, E. L. Hendrickson,, Q. Xia,, T. Wang,, H. Xie,, M. Hackett, and, R. J. Lamont. 2009. Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol. 9:98.
77. Kuboniwa, M.,, G. D. Tribble,, C. E. James,, A. O. Kilic,, L. Tao,, M. C. Herzberg,, S. Shizukuishi, and, R. J. Lamont. 2006. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol. Microbiol. 60:121139.
78. Lamont, R. J.,, A. Chan,, C. M. Belton,, K. T. Izutsu,, D. Vasel, and, A. Weinberg. 1995. Porphyromonas gingivalis invasion of gingival epithelial cells. Infect. Immun. 63:38783885.
79. Lamont, R. J.,, A. El-Sabaeny,, Y. Park,, G. S. Cook,, J. W. Costerton, and, D. R. Demuth. 2002. Role of the Streptococcus gordonii SspB protein in the development of Porphyromonas gingivalis biofilms on streptococcal substrates. Microbiology 148:16271636.
80. Lee, J.,, A. Jayaraman, and, T. K. Wood. 2007. Indole is an inter-species biofilm signal mediated by SdiA. BMC Microbiol. 7:42.
81. Lewis, J. P.,, D. Iyer, and, C. Anaya-Bergman. 2009. Adaptation of Porphyromonas gingivalis to microaerophilic conditions involves increased consumption of formate and reduced utilization of lactate. Microbiology 155:37583774.
82. Li, J.,, E. J. Helmerhorst,, C. W. Leone,, R. F. Troxler,, T. Yaskell,, A. D. Haffajee,, S. S. Socransky, and, F. G. Oppenheim. 2004. Identification of early microbial colonizers in human dental biofilm. J. Appl. Microbiol. 97:13111318.
83. Lin, X.,, R. J. Lamont,, J. Wu, and, H. Xie. 2008. Role of differential expression of streptococcal arginine deiminase in inhibition of fimA expression in Porphyromonas gingivalis. J. Bacteriol. 190:43674371.
84. Maeda, K.,, H. Nagata,, Y. Yamamoto,, M. Tanaka,, J. Tanaka,, N. Minamino, and, S. Shizukuishi. 2004. Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus oralis functions as a coadhesin for Porphyromonas gingivalis major fimbriae. Infect. Immun. 72:13411348.
85. Maeda, K.,, G. D. Tribble,, C. M. Tucker,, C. Anaya,, S. Shizukuishi,, J. P. Lewis,, D. R. Demuth, and, R. J. Lamont. 2008. A Porphyromonas gingivalis tyrosine phosphatase is a multifunctional regulator of virulence attributes. Mol. Microbiol. 69:11531164.
86. Marsh, P. D. 2003. Are dental diseases examples of ecological catastrophes? Microbiology 149:279294.
87. McBride, B. C.,, and J. S. van der Hoeven. 1981. Role of interbacterial adherence in colonization of the oral cavities of gnotobiotic rats infected with Streptococcus mutans and Veillonella alcalescens. Infect. Immun. 33:467472.
88. McNab, R.,, S. K. Ford,, A. El-Sabaeny,, B. Barbieri,, G. S. Cook, and, R. J. Lamont. 2003. LuxS-based signaling in Streptococcus gordonii: autoinducer 2 controls carbohydrate metabolism and biofilm formation with Porphyromonas gingivalis. J. Bacteriol. 185:274284.
89. Meyer, D. H.,, J. E. Lippmann, and, P. M. Fives-Taylor. 1996. Invasion of epithelial cells by Actinobacillus actinomycetemcomitans: a dynamic, multistep process. Infect. Immun. 64:29882997.
90. Mishra, A.,, C. Wu,, J. Yang,, J. O. Cisar,, A. Das, and, H. Ton-That. 2010. The Actinomyces oris type 2 fimbrial shaft FimA mediates coaggregation with oral streptococci, adherence to red blood cells and biofilm development. Mol. Microbiol. 77:841854.
91. Nasidze, I.,, J. Li,, D. Quinque,, K. Tang, and, M. Stoneking. 2009. Global diversity in the human salivary microbiome. Genome Res. 19:636643.
92. Nobbs, A. H.,, R. J. Lamont, and, H. F. Jenkinson. 2009. Streptococcus adherence and colonization. Microbiol. Mol. Biol. Rev. 73:407450.
93. Novak, E. A.,, H. Shao,, C. A. Daep, and, D. R. Demuth. 2010. Autoinducer-2 and QseC control biofilm formation and in vivo virulence of Aggregatibacter actinomycetemcomitans. Infect. Immun. 78:29192926.
94. Nyvad, B.,, and O. Fejerskov. 1987. Scanning electron microscopy of early microbial colonization of human enamel and root surfaces in vivo. Scand. J. Dent. Res. 95:287296.
95. Nyvad, B.,, and M. Kilian. 1987. Microbiology of the early colonization of human enamel and root surfaces in vivo. Scand. J. Dent. Res. 95:369380.
96. Onishi, S.,, K. Honma,, S. Liang,, P. Stathopoulou,, D. Kinane,, G. Hajishengallis, and, A. Sharma. 2008. Toll-like receptor 2-mediated interleukin-8 expression in gingival epithelial cells by the Tannerella forsythia leucine-rich repeat protein BspA. Infect. Immun. 76:198205.
97. Palmer, R. J.,, Jr., P. I. Diaz, and, P. E. Kolenbrander. 2006. Rapid succession within the Veillonella population of a developing human oral biofilm in situ. J. Bacteriol. 188:41174124.
98. Palmer, R. J.,, Jr., S. M. Gordon,, J. O. Cisar, and, P. E. Kolenbrander. 2003. Coaggregation-mediated interactions of streptococci and actinomyces detected in initial human dental plaque. J. Bacteriol. 185:34003409.
99. Palmer, R. J.,, Jr., K. Kazmerzak,, M. C. Hansen, and, P. E. Kolenbrander. 2001. Mutualism versus independence: strategies of mixed-species oral biofilms in vitro using saliva as the sole nutrient source. Infect. Immun. 69:57945804.
100. Park, Y.,, M. R. Simionato,, K. Sekiya,, Y. Murakami,, D. James,, W. Chen,, M. Hackett,, F. Yoshimura,, D. R. Demuth, and, R. J. Lamont. 2005. Short fimbriae of Porphyromonas gingivalis and their role in coadhesion with Streptococcus gordonii. Infect. Immun. 73:39833989.
101. Periasamy, S.,, N. I. Chalmers,, L. Du-Thumm, and, P. E. Kolenbrander. 2009. 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. 75:32503257.
102. Periasamy, S.,, and P. E. Kolenbrander. 2009. Aggregatibacter actinomycetemcomitans builds mutualistic biofilm communities with Fusobacterium nucleatum and Veillonella species in saliva. Infect. Immun. 77:35423551.
103. Periasamy, S.,, and P. E. Kolenbrander. 2010. Central role of the early colonizer Veillonella sp. in establishing multispecies biofilm communities with initial, middle, and late colonizers of enamel. J. Bacteriol. 192:29652972.
104. Periasamy, S.,, and P. E. Kolenbrander. 2009. Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J. Bacteriol. 191:68046811.
105. Peterson, J.,, S. Garges,, M. Giovanni,, P. McInnes,, L. Wang,, J. A. Schloss,, V. Bonazzi,, J. E. McEwen,, K. A. Wetterstrand,, C. Deal,, C. C. Baker,, V. Di Francesco,, T. K. Howcroft,, R. W. Karp,, R. D. Lunsford,, C. R. Wellington,, T. Belachew,, M. Wright,, C. Giblin,, H. David,, M. Mills,, R. Salomon,, C. Mullins,, B. Akolkar,, L. Begg,, C. Davis,, L. Grandison,, M. Humble,, J. Khalsa,, A. R. Little,, H. Peavy,, C. Pontzer,, M. Portnoy,, M. H. Sayre,, P. Starke-Reed,, S. Zakhari,, J. Read,, B. Watson, and, M. Guyer. 2009. The NIH Human Microbiome Project. Genome Res. 19:23172323.
106. Qi, F.,, P. Chen, and, P. W. Caufield. 2001. The group I strain of Streptococcus mutans, UA140, produces both the lantibiotic mutacin I and a nonlantibiotic bacteriocin, mutacin IV. Appl. Environ. Microbiol. 67:1521.
107. Ramsey, M. M.,, and M. Whiteley. 2009. Polymicrobial interactions stimulate resistance to host innate immunity through metabolite perception. Proc. Natl. Acad. Sci. USA 106:15781583.
108. Rickard, A. H.,, R. J. Palmer, Jr.,, D. S. Blehert,, S. R. Campagna,, M. F. Semmelhack,, P. G. Egland,, B. L. Bassler, and, P. E. Kolenbrander. 2006. Autoinducer 2: a concentration-dependent signal for mutualistic bacterial biofilm growth. Mol. Microbiol. 60:14461456.
109. Roy, S.,, C. W. Douglas, and, G. P. Stafford. 2010. A novel sialic acid utilization and uptake system in the periodontal pathogen Tannerella forsythia. J. Bacteriol. 192:22852293.
110. Saito, Y.,, R. Fujii,, K. I. Nakagawa,, H. K. Kuramitsu,, K. Okuda, and, K. Ishihara. 2008. Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol. Immunol. 23:16.
111. Sasaki-Imamura, T.,, A. Yano, and, Y. Yoshida. 2010. Production of indole from Ltryptophan and effects of these compounds on biofilm formation by Fusobacterium nucleatum ATCC 25586. Appl. Environ. Microbiol. 76:42604268.
112. Shao, H.,, and D. R. Demuth. 2010. Quorum sensing regulation of biofilm growth and gene expression by oral bacteria and periodontal pathogens. Periodontol. 2000 52:5367.
113. Shao, H.,, R. J. Lamont, and, D. R. Demuth. 2007. Autoinducer 2 is required for biofilm growth of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect. Immun. 75:42114218.
114. Sharma, A. 2010. Virulence mechanisms of Tannerella forsythia. Periodontol. 2000 54:106116.
115. Sharma, A.,, S. Inagaki,, W. Sigurdson, and, H. K. Kuramitsu. 2005. Synergy between Tannerella forsythia and Fusobacterium nucleatum in biofilm formation. Oral Microbiol. Immunol. 20:3942.
116. Sieuwerts, S.,, D. Molenaar,, S. A. F. T. van Hijum,, M. Beerthuyzen,, M. J. A. Stevens,, P. W. M. Janssen,, C. J. Ingham,, F. A. M. de Bok,, W. M. de Vos, and, J. E. T. van Hylckama Vlieg. 2010. Mixed-culture transcriptome analysis reveals the molecular basis of mixed-culture growth in Streptococcus thermophilus and Lactobacillus bulgaricus. Appl. Environ. Microbiol. 76:77757784.
117. Silverman, R. J.,, A. H. Nobbs,, M. M. Vickerman,, M. E. Barbour, and, H. F. Jenkinson. 2010. Interaction of Candida albicans cell wall Als3 protein with Streptococcus gordonii SspB adhesin promotes development of mixed-species communities. Infect. Immun. 78:46444652.
118. Simionato, M. R.,, C. M. Tucker,, M. Kuboniwa,, G. Lamont,, D. R. Demuth,, G. D. Tribble, and, R. J. Lamont. 2006. Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii. Infect. Immun. 74:64196428.
119. Socransky, S. S.,, A. D. Haffajee,, M. A. Cugini,, C. Smith, and, R. L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25:134144.
120. Takemoto, T.,, M. Ozaki,, M. Shirakawa,, T. Hino, and, H. Okamoto. 1993. Purification of arginine-sensitive hemagglutinin from Fusobacterium nucleatum and its role in coaggregation. J. Periodontal Res. 28:2126.
121. Tribble, G. D.,, and R. J. Lamont. 2010. Bacterial invasion of epithelial cells and spreading in periodontal tissue. Periodontol. 2000 52:6883.
122. Van den Abbeele, P.,, C. Grootaert,, M. Marzorati,, S. Possemiers,, W. Verstraete,, P. Gerard,, S. Rabot,, A. Bruneau,, S. El Aidy,, M. Derrien,, E. Zoetendal,, M. Kleerebezem,, H. Smidt, and, T. Van de Wiele. 2010. Microbial community development in a dynamic gut model is reproducible, colon region specific, and selective for Bacteroidetes and Clostridium cluster IX. Appl. Environ. Microbiol. 76:52375246.
123. van der Mei, H. C.,, M. Rustema-Abbing,, J. de Vries, and, H. J. Busscher. 2008. Bond strengthening in oral bacterial adhesion to salivary conditioning films. Appl. Environ. Microbiol. 74:55115515.
124. Van Oss, C. J. 1995. Hydrophobicity of biosurfaces—origin, quantitative determination and interaction energies. Colloids Surf. B 5:91110.
125. Vroom, J. M.,, K. J. De Grauw,, H. C. Gerritsen,, D. J. Bradshaw,, P. D. Marsh,, G. K. Watson,, J. J. Birmingham, and, C. Allison. 1999. Depth penetration and detection of pH gradients in biofilms by two-photon excitation microscopy. Appl. Environ. Microbiol. 65:35023511.
126. Wang, B. Y.,, J. Wu,, R. J. Lamont,, X. Lin, and, H. Xie. 2009. Negative correlation of distributions of Streptococcus cristatus and Porphyromonas gingivalis in subgingival plaque. J. Clin. Microbiol. 47:39023906.
127. Whittaker, C. J.,, C. M. Klier, and, P. E. Kolenbrander. 1996. Mechanisms of adhesion by oral bacteria. Annu. Rev. Microbiol. 50:513552.
128. Wu, C.,, R. Cichewicz,, Y. Li,, J. Liu,, B. Roe,, J. Ferretti,, J. Merritt, and, F. Qi. 2010. Genomic island TnSmu2 of Streptococcus mutans harbors a nonribosomal peptide synthetasepolyketide synthase gene cluster responsible for the biosynthesis of pigments involved in oxygen and H2O2 tolerance. Appl. Environ. Microbiol. 76:58155826.
129. Wu, H.,, J. E. Lippmann,, J. P. Oza,, M. Zeng,, P. Fives-Taylor, and, N. O. Reich. 2006. Inactivation of DNA adenine methyltransferase alters virulence factors in Actinobacillus actinomycetemcomitans. Oral Microbiol. Immunol. 21:238244.
130. Wu, J.,, and H. Xie. 2010. Role of arginine deiminase of Streptococcus cristatus in Porphyromonas gingivalis colonization. Antimicrob. Agents Chemother. 54:46944698.
131. Xie, H.,, X. Lin,, B. Y. Wang,, J. Wu, and, R. J. Lamont. 2007. Identification of a signalling molecule involved in bacterial intergeneric communication. Microbiology 153:32283234.
132. Yang, J.,, M. Ritchey,, Y. Yoshida,, C. A. Bush, and, J. O. Cisar. 2009. Comparative structural and molecular characterization of ribitol-5-phosphate-containing Streptococcus oralis coaggregation receptor polysaccharides. J. Bacteriol. 191:18911900.
133. Yao, L.,, C. Jermanus,, B. Barbetta,, C. Choi,, P. Verbeke,, D. M. Ojcius, and, O. Yilmaz. 2010. Porphyromonas gingivalis infection sequesters pro-apoptotic Bad through Akt in primary gingival epithelial cells. Mol. Oral Microbiol. 25:89101.
134. Yoshida, Y.,, S. Ganguly,, C. A. Bush, and, J. O. Cisar. 2005. Carbohydrate engineering of the recognition motifs in streptococcal coaggregation receptor polysaccharides. Mol. Microbiol. 58:244256.
135. Zambon, J. J.,, L. A. Christersson, and, J. Slots. 1983. Actinobacillus actinomycetemcomitans in human periodontal disease. Prevalence in patient groups and distribution of biotypes and serotypes within families. J. Periodontol. 54:707711.
136. Zaura, E.,, B. J. Keijser,, S. M. Huse, and, W. Crielaard. 2009. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiol. 9:259.
137. Zhang, Y.,, T. Wang,, W. Chen,, O. Yilmaz,, Y. Park,, I. Y. Jung,, M. Hackett, and, R. J. Lamont. 2005. Differential protein expression by Porphyromonas gingivalis in response to secreted epithelial cell components. Proteomics 5:198211.

This is a required field
Please enter a valid email address
Please check the format of the address you have entered.
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error