The Biofilm Community: Rebels with a Cause

Current Oral Health Reports

Volumn 2, Issue 1, 2015, Pages 48-56

  Aruni, A Wilson ^a   Dou, Yuetan ^a   Mishra, Arunima ^a   Fletcher, Hansel M ^a,b  

^a LOMA LINDA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Kyung Hee University   (South Korea)

Author keywords

Biofilms; Microbial; Non bacterial microbiota; Periodontal disease

Indexed keywords

EID: 84969318537     PISSN: None     EISSN: 21963002     Source Type: Journal    
DOI: 10.1007/s40496-014-0044-5     Document Type: Review

References (94)

1. Dethlefsen L, McFall-Ngai M, Relman DA. An ecological and evolutionary perspective on human-microbe mutualism and disease. Nature. 2007;449:811–8. DOI: 10.1038/nature06245
2. Avila M, Ojcius DM, Yilmaz O. The oral microbiota: living with a permanent guest. DNA Cell Biol. 2009;28:405–11. DOI: 10.1089/dna.2009.0874
3. Said HS, Suda W, Nakagome S, et al. Dysbiosis of salivary microbiota in inflammatory bowel disease and its association with oral immunological biomarkers. DNA Res. 2014;21:15–25. DOI: 10.1093/dnares/dst037
4. Jones ML, Martoni CJ, Ganopolsky JG, et al. The human microbiome and bile acid metabolism: dysbiosis, dysmetabolism, disease and intervention. Expert Opin Biol Ther. 2014;14:467–82. DOI: 10.1517/14712598.2014.880420
5. Bjarnsholt T. Introduction to biofilms. New York: Springer; 2011.
6. Lewis K. Persister cells and the riddle of biofilm survival. Biochemistry (Mosc). 2005;70:267–74. DOI: 10.1007/s10541-005-0111-6
7. Lewis K. Riddle of biofilm resistance. Antimicrob Agents Chemother. 2001;45:999–1007. DOI: 10.1128/AAC.45.4.999-1007.2001
8. Cassai E, Galvan M, Trombelli L, et al. HHV-6, HHV-7, HHV-8 in gingival biopsies from chronic adult periodontitis patients. A case-control study. J Clin Periodontol. 2003;30:184–91. DOI: 10.1034/j.1600-051X.2003.00220.x
9. Kassebaum NJ, Bernabe E, Dahiya M, et al. Global Burden of Severe Periodontitis in 1990-2010: A Systematic Review and Meta-regression. J Dent Res. 2014;93:1045–53. DOI: 10.1177/0022034514552491
10. Bergstrom J. Periodontitis and smoking: an evidence-based appraisal. J Evid Based Dent Pract. 2006;6:33–41. DOI: 10.1016/j.jebdp.2005.12.018
11. Teles R, Teles F, Frias-Lopez J, et al. Lessons learned and unlearned in periodontal microbiology. Periodontol 2000. 2013;62:95–162. DOI: 10.1111/prd.12010
12. Marcotte H, Lavoie MC. Oral microbial ecology and the role of salivary immunoglobulin A. Microbiol Mol Biol Rev. 1998;62:71–109.
13. Brogden KA and Guthmiller JM. Polymicrobial diseases. 2002
14. van Steenbergen TJ, van Winkelhoff AJ, De GJ. Pathogenic synergy: mixed infections in the oral cavity. Antonie Van Leeuwenhoek. 1984;50:789–98. DOI: 10.1007/BF02386241
15. Diaz PI. Microbial diversity and interactions in subgingival biofilm communities. Front Oral Biol. 2012;15:17–40. DOI: 10.1159/000329669
16. Zijnge V, Ammann T, Thurnheer T, et al. Subgingival biofilm structure. Front Oral Biol. 2012;15:1–16. DOI: 10.1159/000329667
17. Hajishengallis G, Darveau RP, Curtis MA. The keystone-pathogen hypothesis. Nat Rev Microbiol. 2012;10:717–25. DOI: 10.1038/nrmicro2873
18. Kolenbrander PE. Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol. 2000;54:413–37. DOI: 10.1146/annurev.micro.54.1.413
19. Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Adv Dent Res. 1994;8:263–71.
20. Marsh PD. Are dental diseases examples of ecological catastrophes? Microbiology. 2003;149:279–94. DOI: 10.1099/mic.0.26082-0
21. Kolenbrander PE, Andersen RN, Blehert DS, et al. Communication among oral bacteria. Microbiol Mol Biol Rev. 2002;66:486–505. DOI: 10.1128/MMBR.66.3.486-505.2002
22. Kolenbrander PE, Palmer Jr RJ, Rickard AH, et al. Bacterial interactions and successions during plaque development. Periodontol 2000. 2006;42:47–79. DOI: 10.1111/j.1600-0757.2006.00187.x
23. Peyyala R, Kirakodu SS, Ebersole JL, et al. Novel model for multispecies biofilms that uses rigid gas-permeable lenses. Appl Environ Microbiol. 2011;77:3413–21. DOI: 10.1128/AEM.00039-11
24. Lemon KP, Earl AM, Vlamakis HC, et al. Biofilm development with an emphasis on Bacillus subtilis. Curr Top Microbiol Immunol. 2008;322:1–16.
25. Jenkinson HF, Lamont RJ. Oral microbial communities in sickness and in health. Trends Microbiol. 2005;13:589–95. DOI: 10.1016/j.tim.2005.09.006
26. Aas JA, Paster BJ, Stokes LN, et al. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol. 2005;43:5721–32. DOI: 10.1128/JCM.43.11.5721-5732.2005
27. Lucas VS, Beighton D, Roberts GJ. Composition of the oral streptococcal flora in healthy children. J Dent. 2000;28:45–50. DOI: 10.1016/S0300-5712(99)00048-2
28. Duran-Pinedo AE, Baker VD, Frias-Lopez J. The periodontal pathogen Porphyromonas gingivalis induces expression of transposases and cell death of Streptococcus mitis in a biofilm model. Infect Immun. 2014;82:3374–82. DOI: 10.1128/IAI.01976-14
29. Mashima I, Nakazawa F. The influence of oral Veillonella species on biofilms formed by Streptococcus species. Anaerobe. 2014;28:54–61. DOI: 10.1016/j.anaerobe.2014.05.003
30. Teles RP, Haffajee AD, Socransky SS. Microbiological goals of periodontal therapy. Periodontol 2000. 2006;42:180–218. DOI: 10.1111/j.1600-0757.2006.00192.x
31. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000. 2005;38:135–87. DOI: 10.1111/j.1600-0757.2005.00107.x
32. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000. 1994;5:78–111. DOI: 10.1111/j.1600-0757.1994.tb00020.x
33. Matarazzo F, Figueiredo LC, Cruz SE, et al. Clinical and microbiological benefits of systemic metronidazole and amoxicillin in the treatment of smokers with chronic periodontitis: a randomized placebo-controlled study. J Clin Periodontol. 2008;35:885–96. DOI: 10.1111/j.1600-051X.2008.01304.x
34. Socransky SS. Relationship of bacteria to the etiology of periodontal disease. J Dent Res. 1970;49:203–22. DOI: 10.1177/00220345700490020401
35. Ritz HL. Microbial population shifts in developing human dental plaque. Arch Oral Biol. 1967;12:1561–8. DOI: 10.1016/0003-9969(67)90190-2
36. Theilade E, Wright WH, Jensen SB, et al. Experimental gingivitis in man. II. A longitudinal clinical and bacteriological investigation. J Periodontal Res. 1966;1:1–13. DOI: 10.1111/j.1600-0765.1966.tb01842.x
37. Haffajee AD, Socransky SS, Patel MR, et al. Microbial complexes in supragingival plaque. Oral Microbiol Immunol. 2008;23:196–205. DOI: 10.1111/j.1399-302X.2007.00411.x
38. Haffajee AD, Teles RP, Patel MR, et al. Factors affecting human supragingival biofilm composition. I. Plaque mass. J Periodontal Res. 2009;44:511–9. DOI: 10.1111/j.1600-0765.2008.01154.x
39. Lee A, Ghaname CB, Braun TM, et al. Bacterial and salivary biomarkers predict the gingival inflammatory profile. J Periodontol. 2012;83:79–89. DOI: 10.1902/jop.2011.110060
40. Li J, Helmerhorst EJ, Leone CW, et al. Identification of early microbial colonizers in human dental biofilm. J Appl Microbiol. 2004;97:1311–8. DOI: 10.1111/j.1365-2672.2004.02420.x
41. Sachdeo A, Haffajee AD, Socransky SS. Biofilms in the edentulous oral cavity. J Prosthodont. 2008;17:348–56. DOI: 10.1111/j.1532-849X.2008.00301.x
42. Teles FR, Teles RP, Sachdeo A, et al. Comparison of microbial changes in early redeveloping biofilms on natural teeth and dentures. J Periodontol. 2012;83:1139–48. DOI: 10.1902/jop.2012.110506
43. Uzel NG, Teles FR, Teles RP, et al. Microbial shifts during dental biofilm re-development in the absence of oral hygiene in periodontal health and disease. J Clin Periodontol. 2011;38:612–20. DOI: 10.1111/j.1600-051X.2011.01730.x
44. Hellstrom MK, Ramberg P, Krok L, et al. The effect of supragingival plaque control on the subgingival microflora in human periodontitis. J Clin Periodontol. 1996;23:934–40. DOI: 10.1111/j.1600-051X.1996.tb00514.x
45. Westfelt E, Rylander H, Dahlen G, et al. The effect of supragingival plaque control on the progression of advanced periodontal disease. J Clin Periodontol. 1998;25:536–41. DOI: 10.1111/j.1600-051X.1998.tb02484.x
46. Ribeiro EP, Bittencourt S, Nociti-Junior FH, et al. The effect of one session of supragingival plaque control on clinical and biochemical parameters of chronic periodontitis. J Appl Oral Sci. 2005;13:275–9. DOI: 10.1590/S1678-77572005000300014
47. Kho P, Smales FC, Hardie JM. The effect of supragingival plaque control on the subgingival microflora. J Clin Periodontol. 1985;12:676–86. DOI: 10.1111/j.1600-051X.1985.tb00939.x
48. Beltrami M, Bickel M, Baehni PC. The effect of supragingival plaque control on the composition of the subgingival microflora in human periodontitis. J Clin Periodontol. 1987;14:161–4. DOI: 10.1111/j.1600-051X.1987.tb00960.x
49. Katsanoulas T, Renee I, Attstrom R. The effect of supragingival plaque control on the composition of the subgingival flora in periodontal pockets. J Clin Periodontol. 1992;19:760–5. DOI: 10.1111/j.1600-051X.1992.tb02167.x
50. Socransky SS, Haffajee AD, Cugini MA, et al. Microbial complexes in subgingival plaque. J Clin Periodontol. 1998;25:134–44. DOI: 10.1111/j.1600-051X.1998.tb02419.x
51. Teles R, Sakellari D, Teles F, et al. Relationships among gingival crevicular fluid biomarkers, clinical parameters of periodontal disease, and the subgingival microbiota. J Periodontol. 2010;81:89–98. DOI: 10.1902/jop.2009.090397
52. Haffajee AD, Teles RP, Patel MR, et al. Factors affecting human supragingival biofilm composition. I. Plaque mass. J Periodontal Res. 2009;44:511–9. DOI: 10.1111/j.1600-0765.2008.01154.x
53. Quirynen M, Bollen CM. The influence of surface roughness and surface-free energy on supra- and subgingival plaque formation in man. A review of the literature. J Clin Periodontol. 1995;22:1–14. DOI: 10.1111/j.1600-051X.1995.tb01765.x
54. Quirynen M, Marechal M, Busscher HJ, et al. The influence of surface free-energy on planimetric plaque growth in man. J Dent Res. 1989;68:796–9. DOI: 10.1177/00220345890680050801
55. Souto R, Silva-Boghossian CM, Colombo AP. Prevalence of Pseudomonas aeruginosa and Acinetobacter spp. in subgingival biofilm and saliva of subjects with chronic periodontal infection. Braz J Microbiol. 2014;45:495–501. DOI: 10.1590/S1517-83822014000200017
56. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol. 2000;27:722–32. DOI: 10.1034/j.1600-051x.2000.027010722.x
57. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol. 2000;27:648–57. DOI: 10.1034/j.1600-051x.2000.027009648.x
58. Griffen AL, Beall CJ, Campbell JH, et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J. 2012;6:1176–85. DOI: 10.1038/ismej.2011.191
59. Mysak J, Podzimek S, Sommerova P, et al. Porphyromonas gingivalis: major periodontopathic pathogen overview. J Immunol Res. 2014;2014:476068. DOI: 10.1155/2014/476068
60. Jentsch HF, Marz D, Kruger M. The effects of stress hormones on growth of selected periodontitis related bacteria. Anaerobe. 2013;24:49–54. DOI: 10.1016/j.anaerobe.2013.09.001
61. Thurnheer T, Belibasakis GN, Bostanci N. Colonisation of gingival epithelia by subgingival biofilms in vitro: role of “red complex” bacteria. Arch Oral Biol. 2014;59:977–86. DOI: 10.1016/j.archoralbio.2014.05.023
62. Abusleme L, Dupuy AK, Dutzan N, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013;7:1016–25. DOI: 10.1038/ismej.2012.174
63. Hojo K, Nagaoka S, Ohshima T, et al. Bacterial interactions in dental biofilm development. J Dent Res. 2009;88:982–90. DOI: 10.1177/0022034509346811
64. Egland PG, Palmer Jr RJ, Kolenbrander PE. Interspecies communication in Streptococcus gordonii-Veillonella atypica biofilms: signaling in flow conditions requires juxtaposition. Proc Natl Acad Sci U S A. 2004;101:16917–22. DOI: 10.1073/pnas.0407457101
65. Brown SA, Whiteley M. A novel exclusion mechanism for carbon resource partitioning in Aggregatibacter actinomycetemcomitans. J Bacteriol. 2007;189:6407–14. DOI: 10.1128/JB.00554-07
66. Mayrand D, McBride BC. Exological relationships of bacteria involved in a simple, mixed anaerobic infection. Infect Immun. 1980;27:44–50.
67. Grenier D, Mayrand D. Studies of mixed anaerobic infections involving Bacteroides gingivalis. Can J Microbiol. 1983;29:612–8. DOI: 10.1139/m83-096
68. Grenier D. Nutritional interactions between two suspected periodontopathogens, Treponema denticola and Porphyromonas gingivalis. Infect Immun. 1992;60:5298–301.
69. Aruni AW, Roy F, Sandberg L, et al. Proteome variation among Filifactor alocis strains. Proteomics. 2012;12:3343–64. DOI: 10.1002/pmic.201200211
70. Aruni AW, Zhang K, Dou Y, et al. Proteome analysis of coinfection of epithelial cells with Filifactor alocis and Porphyromonas gingivalis shows modulation of pathogen and host regulatory pathways. Infect Immun. 2014;82:3261–74. DOI: 10.1128/IAI.01727-14
71. Uematsu H, Sato N, Hossain MZ, et al. Degradation of arginine and other amino acids by butyrate-producing asaccharolytic anaerobic Gram-positive rods in periodontal pockets. Arch Oral Biol. 2003;48:423–9. DOI: 10.1016/S0003-9969(03)00031-1
72. Eley BM, Cox SW. Cathepsin B/L-, elastase-, tryptase-, trypsin- and dipeptidyl peptidase IV-like activities in gingival crevicular fluid: a comparison of levels before and after periodontal surgery in chronic periodontitis patients. J Periodontol. 1992;63:412–7. DOI: 10.1902/jop.1992.63.5.412
73. Bramanti TE, Holt SC. Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50. J Bacteriol. 1991;173:7330–9.
74. Kornman KS, Loesche WJ. Effects of estradiol and progesterone on Bacteroides melaninogenicus and Bacteroides gingivalis. Infect Immun. 1982;35:256–63.
75. Turnbaugh PJ, Ley RE, Hamady M, et al. The human microbiome project. Nature. 2007;449:804–10. DOI: 10.1038/nature06244
76. Chen T, Yu WH, Izard J et al. The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxford). 2010;2010:baq013.
77. Griffen AL, Beall CJ, Firestone ND, et al. CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS One. 2011;6:e19051. DOI: 10.1371/journal.pone.0019051
78. Dewhirst FE, Chen T, Izard J, et al. The human oral microbiome. J Bacteriol. 2010;192:5002–17. DOI: 10.1128/JB.00542-10
79. Saito A, Inagaki S, Ishihara K. Differential ability of periodontopathic bacteria to modulate invasion of human gingival epithelial cells by Porphyromonas gingivalis. Microb Pathog. 2009;47:329–33. DOI: 10.1016/j.micpath.2009.09.012
80. Soro V, Dutton LC, Sprague SV, et al. Axenic Culture of a Candidate Division TM7 Bacterium from the Human Oral Cavity and Biofilm Interactions with Other Oral Bacteria. Appl Environ Microbiol. 2014;80:6480–9. DOI: 10.1128/AEM.01827-14
81. Aruni AW, Roy F, Fletcher HM. Filifactor alocis has virulence attributes that can enhance its persistence under oxidative stress conditions and mediate invasion of epithelial cells by Porphyromonas gingivalis. Infect Immun. 2011;79:3872–86. DOI: 10.1128/IAI.05631-11
82. Fine DH, Markowitz K, Fairlie K et al. A consortium of Aggregatibacter actinomycetemcomitans (Aa), Streptococcus parasanguinis and Filifactor alocis are present in sites prior to bone loss in a longitudinal study of localized aggressive periodontitis. J Clin Microbiol. 2013.
83. Slots J. Human viruses in periodontitis. Periodontol 2000. 2010;53:89–110. DOI: 10.1111/j.1600-0757.2009.00325.x
84. Thoulouze MI, Alcover A. Can viruses form biofilms? Trends Microbiol. 2011;19:257–62. DOI: 10.1016/j.tim.2011.03.002
85. Pais-Correia AM, Sachse M, Guadagnini S, et al. Biofilm-like extracellular viral assemblies mediate HTLV-1 cell-to-cell transmission at virological synapses. Nat Med. 2010;16:83–9. DOI: 10.1038/nm.2065
86. He J, Li Y, Cao Y et al. The oral microbiome diversity and its relation to human diseases. Folia Microbiol (Praha). 2014.
87. Miller CS. Viruses: are they really culprits for periodontal disease? A critical review? J Investig Clin Dent. 2014;5:243. DOI: 10.1111/jicd.12114
88. Maddi A, Scannapieco FA. Oral biofilms, oral and periodontal infections, and systemic disease. Am J Dent. 2013;26:249–54.
89. Cappuyns I, Gugerli P, Mombelli A. Viruses in periodontal disease - a review. Oral Dis. 2005;11:219–29. DOI: 10.1111/j.1601-0825.2005.01123.x
90. Stein RA. Epigenetics–the link between infectious diseases and cancer. JAMA. 2011;305:1484–5. DOI: 10.1001/jama.2011.446
91. Minarovits J. Microbe-induced epigenetic alterations in host cells: the coming era of patho-epigenetics of microbial infections. A review. Acta Microbiol Immunol Hung. 2009;56:1–19. DOI: 10.1556/AMicr.56.2009.1.1
92. Paschos K, Allday MJ. Epigenetic reprogramming of host genes in viral and microbial pathogenesis. Trends Microbiol. 2010;18:439–47. DOI: 10.1016/j.tim.2010.07.003
93. Niller HH, Banati F, Nagy K, et al. Update on microbe- incudced epigenetic changes: bacterial effectors and viral oncogenes. Futur Virol. 2013;8:1111–26. DOI: 10.2217/fvl.13.97
94. McCullers JA. The co-pathogenesis of influenza viruses with bacteria in the lung. Nat Rev Microbiol. 2014;12:252–62. DOI: 10.1038/nrmicro3231