Skip to main content

Advertisement

SpringerLink
Log in

Polymicrobial Biofilm Studies: from Basic Science to Biofilm Control

  • Microbiology (M Klein, Section Editor)
  • Published:
Current Oral Health Reports Aims and scope Submit manuscript

Abstract

Microbes rarely exist as single species planktonic forms as they have been commonly studied in the laboratory. Instead, the vast majority exists as part of complex polymicrobial biofilm communities attached to host and environmental surfaces. The oral cavity represents one of the most diverse and well-studied polymicrobial consortia. Despite a burgeoning field of mechanistic biofilm research within the past decades, our understanding of interactions that occur between microbial members within oral biofilms is still limited. Thus, the primary objective of this review is to focus on polymicrobial biofilm formation, microbial interactions and signaling events that mediate oral biofilm development, consequences of oral hygiene on both local and systemic disease, and potential therapeutic strategies to limit oral dysbiosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance

  1. Filoche S, Wong L, Sissons CH. Oral biofilms: emerging concepts in microbial ecology. J Dent Res. 2010;89(1):8–18. doi:10.1177/0022034509351812.

    Article  CAS  PubMed  Google Scholar 

  2. Segata N, Haake SK, Mannon P, Lemon KP, Waldron L, Gevers D, et al. Composition of the adult digestive tract bacterial microbiome based on seven mouth surfaces, tonsils, throat and stool samples. Genome Biol. 2012;13(6):R42. doi:10.1186/gb-2012-13-6-r42.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Simon-Soro A, Tomas I, Cabrera-Rubio R, Catalan MD, Nyvad B, Mira A. Microbial geography of the oral cavity. J Dent Res. 2013;92(7):616–21. doi:10.1177/0022034513488119.

    Article  CAS  PubMed  Google Scholar 

  4. Kleinberg I, Jenkins GN. The pH of dental plaques in the different areas of the mouth before and after meals and their relationship to the pH and rate of flow of resting saliva. Arch Oral Biol. 1964;9:493–516.

    Article  CAS  PubMed  Google Scholar 

  5. Fejerskov O, Nyvad B, Larsen MJ. Human experimental caries models: intra-oral environmental variability. Adv Dent Res. 1994;8(2):134–43.

    CAS  PubMed  Google Scholar 

  6. Jakubovics NS, Kolenbrander PE. The road to ruin: the formation of disease-associated oral biofilms. Oral Dis. 2010;16(8):729–39. doi:10.1111/j.1601-0825.2010.01701.x.

    Article  CAS  PubMed  Google Scholar 

  7. Kuboniwa M, Lamont RJ. Subgingival biofilm formation. Periodontol 2000. 2010;52(1):38–52. doi:10.1111/j.1600-0757.2009.00311.x.

    Article  PubMed Central  PubMed  Google Scholar 

  8. Rosan B, Lamont RJ. Dental plaque formation. Microbes Infect. 2000;2(13):1599–607.

    Article  CAS  PubMed  Google Scholar 

  9. Lee YH, Zimmerman JN, Custodio W, Xiao Y, Basiri T, Hatibovic-Kofman S, et al. Proteomic evaluation of acquired enamel pellicle during in vivo formation. PLoS One. 2013;8(7):e67919. doi:10.1371/journal.pone.0067919.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  10. Brady LJ, Maddocks SE, Larson MR, Forsgren N, Persson K, Deivanayagam CC, et al. The changing faces of Streptococcus antigen I/II polypeptide family adhesins. Mol Microbiol. 2010;77(2):276–86. doi:10.1111/j.1365-2958.2010.07212.x.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  11. Nobbs AH, Jenkinson HF, Everett DB. Generic determinants of Streptococcus colonization and infection. Infect Genet Evol. 2015;33:361–70. doi:10.1016/j.meegid.2014.09.018.

    Article  CAS  PubMed  Google Scholar 

  12. Nobbs AH, Jenkinson HF, Jakubovics NS. Stick to your gums: mechanisms of oral microbial adherence. J Dent Res. 2011;90(11):1271–8. doi:10.1177/0022034511399096.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Hannig C, Hannig M, Rehmer O, Braun G, Hellwig E, Al-Ahmad A. Fluorescence microscopic visualization and quantification of initial bacterial colonization on enamel in situ. Arch Oral Biol. 2007;52(11):1048–56. doi:10.1016/j.archoralbio.2007.05.006.

    Article  CAS  PubMed  Google Scholar 

  14. Takeuchi H, Yamamoto K. Ultrastructural analysis of structural framework in dental plaque developing on synthetic carbonate apatite applied to human tooth surfaces. Eur J Oral Sci. 2001;109(4):249–59.

    Article  CAS  PubMed  Google Scholar 

  15. Diaz PI, Chalmers NI, Rickard AH, Kong C, Milburn CL, Palmer Jr RJ, et al. Molecular characterization of subject-specific oral microflora during initial colonization of enamel. Appl Environ Microbiol. 2006;72(4):2837–48. doi:10.1128/AEM.72.4.2837-2848.2006.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. Takeshita T, Yasui M, Shibata Y, Furuta M, Saeki Y, Eshima N, et al. Dental plaque development on a hydroxyapatite disk in young adults observed by using a barcoded pyrosequencing approach. Sci Rep. 2015;5:8136. doi:10.1038/srep08136.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  17. Xu H, Dongari-Bagtzoglou A. Shaping the oral mycobiota: interactions of opportunistic fungi with oral bacteria and the host. Curr Opin Microbiol. 2015;26:65–70. doi:10.1016/j.mib.2015.06.002.

    Article  CAS  PubMed  Google Scholar 

  18. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, et al. The human oral microbiome. J Bacteriol. 2010;192(19):5002–17. doi:10.1128/JB.00542-10.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  19. Hardie JM, Bowden GH. Bacterial flora of dental plaque. Br Med Bull. 1975;31(2):131–6.

    CAS  PubMed  Google Scholar 

  20. Paster BJ, Olsen I, Aas JA, Dewhirst FE. The breadth of bacterial diversity in the human periodontal pocket and other oral sites. Periodontol 2000. 2006;42:80–7. doi:10.1111/j.1600-0757.2006.00174.x.

    Article  PubMed  Google Scholar 

  21. Duran-Pinedo AE, Frias-Lopez J. Beyond microbial community composition: functional activities of the oral microbiome in health and disease. Microbes Infect. 2015;17(7):505–16. doi:10.1016/j.micinf.2015.03.014.

    Article  PubMed Central  PubMed  Google Scholar 

  22. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J. 2013;7(5):1016–25. doi:10.1038/ismej.2012.174.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Mark Welch JL, Utter DR, Rossetti BJ, Mark Welch DB, Eren AM, Borisy GG. Dynamics of tongue microbial communities with single-nucleotide resolution using oligotyping. Front Microbiol. 2014;5:568. doi:10.3389/fmicb.2014.00568.

    Article  PubMed Central  PubMed  Google Scholar 

  24. Koh AY, Kohler JR, Coggshall KT, Van Rooijen N, Pier GB. Mucosal damage and neutropenia are required for Candida albicans dissemination. PLoS Pathog. 2008;4(2):e35. doi:10.1371/journal.ppat.0040035.

    Article  PubMed Central  PubMed  Google Scholar 

  25. de Carvalho FG, Silva DS, Hebling J, Spolidorio LC, Spolidorio DM. Presence of mutans streptococci and Candida spp. in dental plaque/dentine of carious teeth and early childhood caries. Arch Oral Biol. 2006;51(11):1024–8. doi:10.1016/j.archoralbio.2006.06.001.

    Article  PubMed  Google Scholar 

  26. Dupuy AK, David MS, Li L, Heider TN, Peterson JD, Montano EA, et al. Redefining the human oral mycobiome with improved practices in amplicon-based taxonomy: discovery of Malassezia as a prominent commensal. PLoS One. 2014;9(3):e90899. doi:10.1371/journal.pone.0090899. One of only two studies to address the fungal species resident in the human mouth (also termed the “oral mycobiome”). Findings demonstrate that Malassezia, a common skin opportunistic pathogen, is a common colonizer of oral tissue.

    Article  PubMed Central  PubMed  Google Scholar 

  27. Ghannoum MA, Jurevic RJ, Mukherjee PK, Cui F, Sikaroodi M, Naqvi A, et al. Characterization of the oral fungal microbiome (mycobiome) in healthy individuals. PLoS Pathog. 2010;6(1):e1000713. doi:10.1371/journal.ppat.1000713.

    Article  PubMed Central  PubMed  Google Scholar 

  28. Bowen WH, Koo H. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 2011;45(1):69–86. doi:10.1159/000324598.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  29. Liao S, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, et al. Streptococcus mutans extracellular DNA is upregulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bacteriol. 2014;196(13):2355–66. doi:10.1128/JB.01493-14.

    Article  PubMed Central  PubMed  Google Scholar 

  30. Svensater G, Borgstrom M, Bowden GH, Edwardsson S. The acid-tolerant microbiota associated with plaque from initial caries and healthy tooth surfaces. Caries Res. 2003;37(6):395–403. doi:73390.

  31. Bowen WH. Dental caries—not just holes in teeth! A perspective. Mol Oral Microbiol. 2015. doi:10.1111/omi.12132.

    PubMed  Google Scholar 

  32. Falsetta ML, Klein MI, Colonne PM, Scott-Anne K, Gregoire S, Pai CH, et al. Symbiotic relationship between Streptococcus mutans and Candida albicans synergizes virulence of plaque biofilms in vivo. Infect Immun. 2014;82(5):1968–81. doi:10.1128/IAI.00087-14.

    Article  PubMed Central  PubMed  Google Scholar 

  33. Vacca-Smith AM, Bowen WH. Binding properties of streptococcal glucosyltransferases for hydroxyapatite, saliva-coated hydroxyapatite, and bacterial surfaces. Arch Oral Biol. 1998;43(2):103–10.

    Article  CAS  PubMed  Google Scholar 

  34. Hannig C, Ruggeri A, Al-Khayer B, Schmitz P, Spitzmuller B, Deimling D, et al. Electron microscopic detection and activity of glucosyltransferase B, C, and D in the in situ formed pellicle. Arch Oral Biol. 2008;53(11):1003–10. doi:10.1016/j.archoralbio.2008.04.005.

    Article  CAS  PubMed  Google Scholar 

  35. Klinke T, Kneist S, de Soet JJ, Kuhlisch E, Mauersberger S, Forster A, et al. Acid production by oral strains of Candida albicans and Lactobacilli. Caries Res. 2009;43(2):83–91. doi:10.1159/000204911.

    Article  CAS  PubMed  Google Scholar 

  36. Zero DT, Fontana M, Martinez-Mier EA, Ferreira-Zandona A, Ando M, Gonzalez-Cabezas C, et al. The biology, prevention, diagnosis and treatment of dental caries: scientific advances in the United States. J Am Dent Assoc. 2009;140 Suppl 1:25S–34S.

    Article  CAS  PubMed  Google Scholar 

  37. Islam B, Khan SN, Khan AU. Dental caries: from infection to prevention. Med Sci Monit. 2007;13(11):RA196–203.

    PubMed  Google Scholar 

  38. Raja M, Hannan A, Ali K. Association of oral candidal carriage with dental caries in children. Caries Res. 2010;44(3):272–6. doi:10.1159/000314675.

    Article  CAS  PubMed  Google Scholar 

  39. Jarosz LM, Deng DM, van der Mei HC, Crielaard W, Krom BP. Streptococcus mutans competence-stimulating peptide inhibits Candida albicans hypha formation. Eukaryot Cell. 2009;8(11):1658–64. doi:10.1128/EC.00070-09.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  40. Petersen PE, Bourgeois D, Ogawa H, Estupinan-Day S, Ndiaye C. The global burden of oral diseases and risks to oral health. Bull World Health Organ. 2005;83(9):661–9. doi:/S0042-96862005000900011.

  41. Sztajer H, Szafranski SP, Tomasch J, Reck M, Nimtz M, Rohde M, et al. Cross-feeding and interkingdom communication in dual-species biofilms of Streptococcus mutans and Candida albicans. ISME J. 2014;8(11):2256–71. doi:10.1038/ismej.2014.73.

    Article  CAS  PubMed  Google Scholar 

  42. Jin LJ, Armitage GC, Klinge B, Lang NP, Tonetti M, Williams RC. Global oral health inequalities: task group—periodontal disease. Adv Dent Res. 2011;23(2):221–6. doi:10.1177/0022034511402080.

    Article  CAS  PubMed  Google Scholar 

  43. Handfield M, Baker HV, Lamont RJ. Beyond good and evil in the oral cavity: insights into host-microbe relationships derived from transcriptional profiling of gingival cells. J Dent Res. 2008;87(3):203–23.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  44. Offenbacher S, Barros SP, Paquette DW, Winston JL, Biesbrock AR, Thomason RG, et al. Gingival transcriptome patterns during induction and resolution of experimental gingivitis in humans. J Periodontol. 2009;80(12):1963–82. doi:10.1902/jop.2009.080645.

    Article  CAS  PubMed  Google Scholar 

  45. Sharma N, Charles CH, Lynch MC, Qaqish J, McGuire JA, Galustians JG, et al. Adjunctive benefit of an essential oil-containing mouthrinse in reducing plaque and gingivitis in patients who brush and floss regularly: a six-month study. J Am Dent Assoc. 2004;135(4):496–504.

    Article  CAS  PubMed  Google Scholar 

  46. van der Weijden GA, Timmerman MF, Piscaer M, Snoek I, van der Velden U, Galgut PN. Effectiveness of an electrically active brush in the removal of overnight plaque and treatment of gingivitis. J Clin Periodontol. 2002;29(8):699–704.

    Article  PubMed  Google Scholar 

  47. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol. 2010;8(7):481–90. doi:10.1038/nrmicro2337.

    Article  CAS  PubMed  Google Scholar 

  48. Loesche W. Dental caries and periodontitis: contrasting two infections that have medical implications. Infect Dis Clin N Am. 2007;21(2):471–502. doi:10.1016/j.idc.2007.03.006.

    Article  Google Scholar 

  49. Ramseier CA, Kinney JS, Herr AE, Braun T, Sugai JV, Shelburne CA, et al. Identification of pathogen and host-response markers correlated with periodontal disease. J Periodontol. 2009;80(3):436–46. doi:10.1902/jop.2009.080480.

    Article  CAS  PubMed  Google Scholar 

  50. Sheiham A. Is the chemical prevention of gingivitis necessary to prevent severe periodontitis? Periodontol 2000. 1997;15:15–24.

    Article  CAS  PubMed  Google Scholar 

  51. Kumar PS, Griffen AL, Barton JA, Paster BJ, Moeschberger ML, Leys EJ. New bacterial species associated with chronic periodontitis. J Dent Res. 2003;82(5):338–44.

    Article  CAS  PubMed  Google Scholar 

  52. Pozhitkov AE, Leroux BG, Randolph TW, Beikler T, Flemmig TF, Noble PA. Towards microbiome transplant as a therapy for periodontitis: an exploratory study of periodontitis microbial signature contrasted by oral health, caries and edentulism. BMC Oral Health. 2015;15(1):125. doi:10.1186/s12903-015-0109-4.

    Article  PubMed Central  PubMed  Google Scholar 

  53. Huang S, Li R, Zeng X, He T, Zhao H, Chang A, et al. Predictive modeling of gingivitis severity and susceptibility via oral microbiota. ISME J. 2014;8(9):1768–80. doi:10.1038/ismej.2014.32.

    Article  PubMed Central  PubMed  Google Scholar 

  54. Beikler T, Prior K, Ehmke B, Flemmig TF. Specific antibiotics in the treatment of periodontitis—a proposed strategy. J Periodontol. 2004;75(1):169–75. doi:10.1902/jop.2004.75.1.169.

    Article  PubMed  Google Scholar 

  55. Yost S, Duran-Pinedo AE, Teles R, Krishnan K, Frias-Lopez J. Functional signatures of oral dysbiosis during periodontitis progression revealed by microbial metatranscriptome analysis. Genome Med. 2015;7(1):27. doi:10.1186/s13073-015-0153-3-153.

    Article  PubMed Central  PubMed  Google Scholar 

  56. Potera C. Forging a link between biofilms and disease. Science. 1999;283(5409):1837–9.

    Article  CAS  PubMed  Google Scholar 

  57. Papapanou PN. Systemic effects of periodontitis: lessons learned from research on atherosclerotic vascular disease and adverse pregnancy outcomes. Int Dent J. 2015. doi:10.1111/idj.12185.

    PubMed  Google Scholar 

  58. Lu Q, Jin L. Human gingiva is another site of C-reactive protein formation. J Clin Periodontol. 2010;37(9):789–96. doi:10.1111/j.1600-051X.2010.01600.x.

    Article  CAS  PubMed  Google Scholar 

  59. Chen Z, Potempa J, Polanowski A, Wikstrom M, Travis J. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J Biol Chem. 1992;267(26):18896–901.

    CAS  PubMed  Google Scholar 

  60. Kadowaki T, Nakayama K, Yoshimura F, Okamoto K, Abe N, Yamamoto K. Arg-gingipain acts as a major processing enzyme for various cell surface proteins in Porphyromonas gingivalis. J Biol Chem. 1998;273(44):29072–6.

    Article  CAS  PubMed  Google Scholar 

  61. Guo Y, Nguyen KA, Potempa J. Dichotomy of gingipains action as virulence factors: from cleaving substrates with the precision of a surgeon’s knife to a meat chopper-like brutal degradation of proteins. Periodontol 2000. 2010;54(1):15–44. doi:10.1111/j.1600-0757.2010.00377.x.

    Article  PubMed Central  PubMed  Google Scholar 

  62. Silman AJ, Pearson JE. Epidemiology and genetics of rheumatoid arthritis. Arthritis Res. 2002;4 Suppl 3:S265–S72.

    Article  PubMed Central  PubMed  Google Scholar 

  63. Turesson C, McClelland RL, Christianson TJ, Matteson EL. Multiple extra-articular manifestations are associated with poor survival in patients with rheumatoid arthritis. Ann Rheum Dis. 2006;65(11):1533–4. doi:10.1136/ard.2006.052803.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  64. Brown LJ, Loe H. Prevalence, extent, severity and progression of periodontal disease. Periodontol 2000. 1993;2:57–71.

    Article  CAS  PubMed  Google Scholar 

  65. Kharlamova N, Jiang X, Sherina N, Potempa B, Israelsson L, Quirke AM, et al. Antibodies to Porphyromonas gingivalis indicate interaction between oral infection, smoking and risk genes in rheumatoid arthritis etiology. Arthritis Rheum. 2015. doi:10.1002/art.39491. Findings from this associative clinical study suggest that the periodontal pathogen Porphyromonas gingivalis drives production of anti-citrullinated protein antibodies (ACPA) linked with rheumatoid arthritis.

  66. Rantapaa-Dahlqvist S, de Jong BA, Berglin E, Hallmans G, Wadell G, Stenlund H, et al. Antibodies against cyclic citrullinated peptide and IgA rheumatoid factor predict the development of rheumatoid arthritis. Arthritis Rheum. 2003;48(10):2741–9. doi:10.1002/art.11223.

    Article  PubMed  Google Scholar 

  67. Rosenstein ED, Greenwald RA, Kushner LJ, Weissmann G. Hypothesis: the humoral immune response to oral bacteria provides a stimulus for the development of rheumatoid arthritis. Inflammation. 2004;28(6):311–8. doi:10.1007/s10753-004-6641-z.

    Article  PubMed  Google Scholar 

  68. Trevisan M, Dorn J. The relationship between periodontal disease (pd) and cardiovascular disease (cvd). Mediterr J Hematol Infect Dis. 2010;2(3):e2010030. doi:10.4084/MJHID.2010.030.

    Article  PubMed Central  PubMed  Google Scholar 

  69. Oktay S, Chukkapalli SS, Rivera-Kweh MF, Velsko IM, Holliday LS, Kesavalu L. Periodontitis in rats induces systemic oxidative stress that is controlled by bone-targeted antiresorptives. J Periodontol. 2015;86(1):137–45. doi:10.1902/jop.2014.140302.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  70. Paquette DW, Brodala N, Nichols TC. Cardiovascular disease, inflammation, and periodontal infection. Periodontol 2000. 2007;44:113–26. doi:10.1111/j.1600-0757.2006.00196.x.

    Article  PubMed  Google Scholar 

  71. Gangula P, Ravella K, Chukkapalli S, Rivera M, Srinivasan S, Hale A, et al. Polybacterial periodontal pathogens alter vascular and gut BH4/nNOS/NRF2-phase II enzyme expression. PLoS One. 2015;10(6):e0129885. doi:10.1371/journal.pone.0129885.

    Article  PubMed Central  PubMed  Google Scholar 

  72. Reichert S, Schlitt A, Beschow V, Lutze A, Lischewski S, Seifert T, et al. Use of floss/interdental brushes is associated with lower risk for new cardiovascular events among patients with coronary heart disease. J Periodontal Res. 2015;50(2):180–8. doi:10.1111/jre.12191. Findings from this study suggest that flossing and brushing of interdental spaces may reduce the incidence of future cardiovascular event among patients with coronary heart disease, further emphasizing the role of oral pathogens in systemic disease.

    Article  CAS  PubMed  Google Scholar 

  73. Serra e Silva Filho W, Casarin RC, Nicolela Jr EL, Passos HM, Sallum AW, Goncalves RB. Microbial diversity similarities in periodontal pockets and atheromatous plaques of cardiovascular disease patients. PLoS One. 2014;9(10):e109761. doi:10.1371/journal.pone.0109761. The objective of this study was to use 16S-based sequencing approaches to examine the microbial diversity in the subgingival plaque and atheroma plaques of patients with gingivitis and coronary artery atherosclerosis. Microbial compositions between these anatomical sites were highly conserved, further suggesting that oral plaque may translocate to seed infection at distant biological sites.

    Article  PubMed Central  PubMed  Google Scholar 

  74. Velsko IM, Chukkapalli SS, Rivera MF, Lee JY, Chen H, Zheng D, et al. Active invasion of oral and aortic tissues by Porphyromonas gingivalis in mice causally links periodontitis and atherosclerosis. PLoS One. 2014;9(5):e97811. doi:10.1371/journal.pone.0097811PONE-D-13-52626.

    Article  PubMed Central  PubMed  Google Scholar 

  75. Janket SJ, Javaheri H, Ackerson LK, Ayilavarapu S, Meurman JH. Oral infections, metabolic inflammation, genetics, and cardiometabolic diseases. J Dent Res. 2015;94(9 Suppl):119S–27S. doi:10.1177/0022034515580795.

    Article  PubMed  Google Scholar 

  76. Schlecht LM, Peters BM, Krom BP, Freiberg JA, Hansch GM, Filler SG, et al. Systemic Staphylococcus aureus infection mediated by Candida albicans hyphal invasion of mucosal tissue. Microbiology. 2015;161(Pt 1):168–81. doi:10.1099/mic.0.083485-0. Findings from this study revealed that the under-represented oral colonizer, Staphylococcus aureus, can utilize the invasive hyphal filaments of the common oral fungus Candida albicans to disseminate and cause lethal systemic staphylococcal infection in a murine model. This study builds on the growing appreciation for fungi and bacteria to interact in vivo, often resulting in infectious synergism.

  77. Peters BM, Ovchinnikova ES, Krom BP, Schlecht LM, Zhou H, Hoyer LL, et al. Staphylococcus aureus adherence to Candida albicans hyphae is mediated by the hyphal adhesin Als3p. Microbiology. 2012;158(Pt 12):2975–86. doi:10.1099/mic.0.062109-0.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  78. Temoin S, Chakaki A, Askari A, El-Halaby A, Fitzgerald S, Marcus RE, et al. Identification of oral bacterial DNA in synovial fluid of patients with arthritis with native and failed prosthetic joints. J Clin Rheumatol. 2012;18(3):117–21. doi:10.1097/RHU.0b013e3182500c95.

    Article  PubMed Central  PubMed  Google Scholar 

  79. Anbinder AL, Moraes RM, Lima GM, Oliveira FE, Campos DR, Rossoni RD, et al. Periodontal disease exacerbates systemic ovariectomy-induced bone loss in mice. Bone. 2015. doi:10.1016/j.bone.2015.11.014.

    PubMed  Google Scholar 

  80. Benedyk M, Mydel PM, Delaleu N, Plaza K, Gawron K, Milewska A, et al. Gingipains: critical factors in the development of aspiration pneumonia caused by Porphyromonas gingivalis. J Innate Immun. 2015. doi:10.1159/000441724.

    PubMed  Google Scholar 

  81. Hall-Stoodley L, Costerton JW, Stoodley P. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol. 2004;2(2):95–108. doi:10.1038/nrmicro821.

    Article  CAS  PubMed  Google Scholar 

  82. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol. 2010;8(1):15–25. doi:10.1038/nrmicro2259.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  83. Rickard AH, Gilbert P, High NJ, Kolenbrander PE, Handley PS. Bacterial coaggregation: an integral process in the development of multi-species biofilms. Trends Microbiol. 2003;11(2):94–100.

    Article  CAS  PubMed  Google Scholar 

  84. Stewart PS, Franklin MJ. Physiological heterogeneity in biofilms. Nat Rev Microbiol. 2008;6(3):199–210. doi:10.1038/nrmicro1838.

    Article  CAS  PubMed  Google Scholar 

  85. Leung V, Dufour D, Levesque CM. Death and survival in Streptococcus mutans: differing outcomes of a quorum-sensing signaling peptide. Front Microbiol. 2015;6:1176. doi:10.3389/fmicb.2015.01176.

    Article  PubMed Central  PubMed  Google Scholar 

  86. Ng WL, Bassler BL. Bacterial quorum-sensing network architectures. Annu Rev Genet. 2009;43:197–222. doi:10.1146/annurev-genet-102108-134304.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  87. Jack AA, Daniels DE, Jepson MA, Vickerman MM, Lamont RJ, Jenkinson HF, et al. Streptococcus gordonii comCDE (competence) operon modulates biofilm formation with Candida albicans. Microbiology. 2015;161(Pt 2):411–21. doi:10.1099/mic.0.000010.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  88. Scheres N, Lamont RJ, Crielaard W, Krom BP. LuxS signaling in Porphyromonas gingivalis-host interactions. Anaerobe. 2015;35(Pt A):3–9. doi:10.1016/j.anaerobe.2014.11.011.

    Article  CAS  PubMed  Google Scholar 

  89. Bachtiar EW, Bachtiar BM, Jarosz LM, Amir LR, Sunarto H, Ganin H, et al. AI-2 of Aggregatibacter actinomycetemcomitans inhibits Candida albicans biofilm formation. Front Cell Infect Microbiol. 2014;4:94. doi:10.3389/fcimb.2014.00094.

    Article  PubMed Central  PubMed  Google Scholar 

  90. Jang YJ, Sim J, Jun HK, Choi BK. Differential effect of autoinducer 2 of Fusobacterium nucleatum on oral streptococci. Arch Oral Biol. 2013;58(11):1594–602. doi:10.1016/j.archoralbio.2013.08.006.

    Article  CAS  PubMed  Google Scholar 

  91. Lamont RJ, Hajishengallis G. Polymicrobial synergy and dysbiosis in inflammatory disease. Trends Mol Med. 2015;21(3):172–83. doi:10.1016/j.molmed.2014.11.004.

    Article  CAS  PubMed  Google Scholar 

  92. Hans M, Madaan Hans V. Epithelial antimicrobial peptides: guardian of the oral cavity. Int J Pept. 2014;2014:370297. doi:10.1155/2014/370297.

    Article  PubMed Central  PubMed  Google Scholar 

  93. Kasper SH, Samarian D, Jadhav AP, Rickard AH, Musah RA, Cady NC. S-aryl-L-cysteine sulphoxides and related organosulphur compounds alter oral biofilm development and AI-2-based cell-cell communication. J Appl Microbiol. 2014;117(5):1472–86. doi:10.1111/jam.12616.

    Article  CAS  PubMed  Google Scholar 

  94. Ryan EM, Gorman SP, Donnelly RF, Gilmore BF. Recent advances in bacteriophage therapy: how delivery routes, formulation, concentration and timing influence the success of phage therapy. J Pharm Pharmacol. 2011;63(10):1253–64. doi:10.1111/j.2042-7158.2011.01324.x.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Clinical Pharmacy, College of Pharmacy, University of Tennessee Health Sciences Center, 881 Madison Ave, Rm 341, Memphis, TN, 38163, USA

    Hubertine ME Willems & Brian M Peters

  2. Department of Microbiology, Immunology, and Biochemistry, University of Tennessee Health Sciences Center, 858 Madison Ave, Memphis, TN, 38163, USA

    Brian M Peters

  3. College of Light Industry and Food Sciences, South China University of Technology, Guangzhou, 510640, China

    Zhenbo Xu

Authors
  1. Hubertine ME Willems
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Zhenbo Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brian M Peters
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Brian M Peters.

Ethics declarations

Conflict of Interest

Hubertine ME Willems, Zhenbo Xu, and Brian M Peters declare that they have no conflict of interest.

Human and Animal Rights and Informed Consent

This article does not contain any studies with human or animal subjects performed by any of the authors.

Additional information

This article is part of the Topical Collection on Microbiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Willems, H.M., Xu, Z. & Peters, B.M. Polymicrobial Biofilm Studies: from Basic Science to Biofilm Control. Curr Oral Health Rep 3, 36–44 (2016). https://doi.org/10.1007/s40496-016-0078-y

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40496-016-0078-y

Keywords

Search

Navigation