Skip to main content

Exposure of Streptococcus mutans and Streptococcus sanguinis to blue light in an oral biofilm model

Abstract

The potential anti-cariogenic effect of blue light was evaluated using an oral biofilm model. Two species, Streptococcus mutans and Streptococcus sanguinis, were cultivated ex vivo on bovine enamel blocks for 24 h, either separately or mixed together, then exposed to blue light (wavelengths 400–500 nm) using 112 J/cm2. Twenty four or 48 h after exposure to light the biofilm structure and biomass were characterized and quantified using SEM and qPCR, respectively. Bacterial viability was analyzed by CLSM using live/dead bacterial staining. Gene expression was examined by RT-qPCR. After exposure to light, S. mutans biomass in mono-species biofilm was increased mainly by dead bacteria, relative to control. However, the bacterial biomass of S. mutans when grown in mixed biofilm and of S. sanguinis in mono-species biofilm was reduced after light exposure, with no significant change in viability when compared to control. Furthermore, when grown separately, an upregulation of gene expression related to biofilm formation of S. mutans, and downregulation of similar genes of S. sanguinis, were measured 24 h after exposure to blue light. However, in mixed biofilm, a downregulation of those genes in both species was observed, although not significant in S. mutans. In conclusion, blue light seems to effectively alter the bacterial biomass by reducing the viability and virulence characteristics in both bacterial species and may promote the anti-cariogenic balance between them, when grown in a mixed biofilm. Therefore, exposure of oral biofilm to blue light has the potential to serve as a complementary approach in preventive dentistry.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  1. Pitts NB, Zero DT, Marsh PD, Ekstrand K, Weintraub JA, Ramos-Gomez F, Tagami J, Twetman S, Tsakos G, Ismail A (2017) Dental caries. Nat Rev Dis Primers 3:17030

    PubMed  Article  Google Scholar 

  2. Marsh PD (2005) Dental plaque: biological significance of a biofilm and community life-style. J Clin Periodontol 32(Suppl 6):7–15

    CAS  PubMed  Article  Google Scholar 

  3. Steinberg D, Moreinos D, Featherstone J, Shemesh M, Feuerstein O (2008) Genetic and physiological effects of noncoherent visible light combined with hydrogen peroxide on Streptococcus mutans in biofilm. Antimicrob Agents Chemother 52(7):2626–2631

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  4. Larsen T, Fiehn NE (2017) Dental biofilm infections – an update. APMIS 125(4):376–384

    CAS  PubMed  Article  Google Scholar 

  5. Niven CF Jr, White JC (1946) A study of streptococci associated with subacute bacterial endocarditis. J Bacteriol 51(6):790

    PubMed  PubMed Central  Article  Google Scholar 

  6. Ge Y, Caufield PW, Fisch GS, Li Y (2008) Streptococcus mutans and Streptococcus sanguinis colonization correlated with caries experience in children. Caries Res 42(6):444–448

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  7. Valdebenito B, Tullume-Vergara PO, González W, Kreth J, Giacaman RA (2017) In silico analysis of the competition between Streptococcus sanguinis and Streptococcus mutans in the dental biofilm. Mol Oral Microbiol 33(2):168–180

    Article  CAS  Google Scholar 

  8. Kreth J, Merritt J, Qi F (2009) Bacterial and host interactions of oral streptococci. DNA Cell Biol 28(8):397–403

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Feuerstein O, Persman N, Weiss EI (2004) Phototoxic effect of visible light on Porphyromonas gingivalis and Fusobacterium nucleatum: An in Vitro Study. Photochem Photobiol 80(3):412–415

    CAS  PubMed  Article  Google Scholar 

  10. Chebath-Taub D, Steinberg D, Featherstone JD, Feuerstein O (2012) Influence of blue light on Streptococcus mutans re-organization in biofilm. J Photochem Photobiol B 116:75–78

    CAS  PubMed  Article  Google Scholar 

  11. Sol A, Feuerstein O, Featherstone JD, Steinberg D (2011) Effect of sublethal CO2 laser irradiation on gene expression of Streptococcus mutans immobilized in a biofilm. Caries Res 45(4):361–369

    CAS  PubMed  Article  Google Scholar 

  12. Cohen-Berneron J, Steinberg D, Featherstone JD, Feuerstein O (2016) Sustained effects of blue light on Streptococcus mutans in regrown biofilm. Lasers Med Sci 31(3):445–452

    PubMed  Article  Google Scholar 

  13. Feuerstein O, Assad R, Koren E, Ginsburg I, Weiss EI, Houri-Haddad Y (2011) Visible light promotes interleukin-10 secretion by sublethal fluences. Photomed Laser Surg. 29(9):627–633

    CAS  PubMed  Article  Google Scholar 

  14. McCormack SM, Fried D, Featherstone JD, Glena RE, Seka W (1995) Scanning electron microscope observations of CO2 laser effects on dental enamel. J Dent Res 74(10):1702–1708

    CAS  PubMed  Article  Google Scholar 

  15. Periasamy S, Kolenbrander PE (2009) Mutualistic biofilm communities develop with Porphyromonas gingivalis and initial, early, and late colonizers of enamel. J Bacteriol 191(22):6804–6811

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  16. Assaf D, Steinberg D, Shemesh M (2015) Lactose triggers biofilm formation by Streptococcus mutans. Int Dairy J 42:51–57

    CAS  Article  Google Scholar 

  17. Shemesh M, Tam A, Aharoni R, Steinberg D (2010) Genetic adaptation of Streptococcus mutans during biofilm formation on different types of surfaces. BMC Microbiol 10:51

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  18. Feldman M, Al-Quntar A, Polacheck I, Friedman M, Steinberg D (2014) Therapeutic potential of thiazolidinedione-8 as an antibiofilm agent against Candida albicans. PLoS One 9(5):e93225

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  19. Ramage G, Saville SP, Wickes BL, López-Ribot JL (2002) Inhibition of Candida albicans biofilm formation by farnesol, a quorum-sensing molecule. Appl Environ Microbiol 68(11):5459–5463

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  20. Shemesh M, Tam A, Steinberg D (2007) Differential gene expression profiling of Streptococcus mutans cultured under biofilm and planktonic conditions. Microbiology 153(Pt 5):1307–1317

    CAS  PubMed  Article  Google Scholar 

  21. Shemesh M, Tam A, Feldman M, Steinberg D (2006) Differential expression profiles of Streptococcus mutans ftf, gtf and vicR genes in the presence of dietary carbohydrates at early and late exponential growth phases. Carbohydr Res 341(12):2090–2097

    CAS  PubMed  Article  Google Scholar 

  22. Kreth J, Giacaman RA, Raghavan R, Merritt J (2017) The road less traveled – defining molecular commensalism with Streptococcus sanguinis. Mol Oral Microbiol 32(3):181–196

    CAS  PubMed  Article  Google Scholar 

  23. Cieplik F, Kara E, Muehler D, Enax J, Hiller KA, Maisch T, Buchalla W (2018) Antimicrobial efficacy of alternative compounds for use in oral care toward biofilms from caries-associated bacteria in vitro. Microbiologyopen e00695

  24. Krzyściak W, Jurczak A, Kościelniak D, Bystrowska B, Skalniak A (2014) The virulence of Streptococcus mutans and the ability to form biofilms. Eur J Clin Microbiol Infect Dis 33(4):499–515

    PubMed  Article  Google Scholar 

  25. Rossoni RD, Velloso MDS, de Barros PP, de Alvarenga JA, Santos JDD, Santos Prado ACCD, Ribeiro FC, Anbinder AL, Junqueira JC (2018) Inhibitory effect of probiotic Lactobacillus supernatants from the oral cavity on Streptococcus mutans biofilms. Microb Pathog 123:361–367

    PubMed  Article  Google Scholar 

  26. Souza JGS, Cury JA, Ricomini Filho AP, Feres M, Faveri M, Barão VAR (2018) Effect of sucrose on biofilm formed in situ on titanium material. J Periodontol

  27. Feuerstein O (2012) Light therapy: complementary antibacterial treatment of oral biofilm. Adv Dent Res 24(2):103–107

    CAS  PubMed  Article  Google Scholar 

  28. Palma ALDR, Ramos LP, Domingues N, Back-Brito GN, de Oliveira LD, Pereira CA, Jorge AOC (2018) Biofilms of Candida albicans and Streptococcus sanguinis and their susceptibility to antimicrobial effects of photodynamic inactivation. Photodiagnosis Photodyn Ther pii S1572-1000(17):30455–30456

    Google Scholar 

  29. Hauser-Gerspach I, Stübinger S, Meyer J (2010) Bactericidal effects of different laser systems on bacteria adhered to dental implant surfaces: an in vitro study comparing zirconia with titanium. Clin Oral Implants Res 21(3):277–283

    PubMed  Article  Google Scholar 

  30. Uchinuma S, Shimada Y, Matin K, Hosaka K, Yoshiyama M, Sumi Y, Tagami J (2018) Effects of UVB and UVC irradiation on cariogenic bacteria in vitro. Lasers Med Sci. https://doi.org/10.1007/s10103-018-2685-4

    PubMed  Article  Google Scholar 

  31. Giusti JS, Santos-Pinto L, Pizzolito AC, Helmerson K, Carvalho-Filho E, Kurachi C, Bagnato VS (2008) Antimicrobial photodynamic action on dentin using a light-emitting diode light source. Photomed Laser Surg 26(4):281–287

    PubMed  Article  Google Scholar 

  32. Hakimiha N, Khoei F, Bahador A, Fekrazad R (2014) The susceptibility of Streptococcus mutans to antibacterial photodynamic therapy: a comparison of two different photosensitizers and light sources. J Appl Oral Sci 22(2):80–84

    PubMed  PubMed Central  Article  Google Scholar 

  33. Pereira CA, Costa AC, Carreira CM, Junqueira JC, Jorge AO (2013) Photodynamic inactivation of Streptococcus mutans and Streptococcus sanguinis biofilms in vitro. Lasers Med Sci 28(3):859–864

    PubMed  Article  Google Scholar 

  34. Soria-Lozano P, Gilaberte Y, Paz-Cristobal MP, Pérez-Artiaga L, Lampaya-Pérez V, Aporta J, Pérez-Laguna V, García-Luque I, Revillo MJ, Rezusta A (2015) In vitro effect photodynamic therapy with differents photosensitizers on cariogenic microorganisms. BMC Microbiol 15:187

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  35. Pérez-Laguna V, Pérez-Artiaga L, Lampaya-Pérez V, López SC, García-Luque I, Revillo MJ, Nonell S, Gilaberte Y, Rezusta A (2017) Comparative effect of photodynamic therapy on separated or mixed cultures of Streptococcus mutans and Streptococcus sanguinis. Photodiagnosis Photodyn Ther 19:98–102

    PubMed  Article  CAS  Google Scholar 

  36. Ichinose-Tsuno A, Aoki A, Takeuchi Y, Kirikae T, Shimbo T, Lee MC, Yoshino F, Maruoka Y, Itoh T, Ishikawa I, Izumi Y (2014) Antimicrobial photodynamic therapy suppresses dental plaque formation in healthy adults: a randomized controlled clinical trial. BMC Oral Health 14:152

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  37. Feuerstein O, Ginsburg I, Dayan E, Veler D, Weiss EI (2005) Mechanism of visible light phototoxicity on Porphyromonas gingivalis and Fusobacterium nucleatum. Photochem Photobiol 81(5):1186–1189

    CAS  PubMed  Article  Google Scholar 

  38. Sterer N, Feuerstein O (2005) Effect of visible light on malodour production by mixed oral microflora. J Med Microbiol 54(Pt 12):1225–1229

    CAS  PubMed  Article  Google Scholar 

  39. Khaengraeng R, Reed RH (2005) Oxygen and photoinactivation of Escherichia coli in UVA and sunlight. J Appl Microbiol 99(1):39–50

    CAS  PubMed  Article  Google Scholar 

  40. Lubart R, Lipovski A, Nitzan Y, Friedmann H (2011) A possible mechanism for the bactericidal effect of visible light. Laser Ther 20(1):17–22

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  41. Storz G, Imlay JA (1999) Oxidative stress. Curr Opin Microbiol 2(2):188–194

    CAS  PubMed  Article  Google Scholar 

  42. Tardu M, Bulut S, Kavakli IH (2017) MerR and ChrR mediate blue light induced photo-oxidative stress response at the transcriptional level in Vibrio cholerae. Sci Rep 18(7):40817

    Article  CAS  Google Scholar 

  43. Chui C, Hiratsuka K, Aoki A, Takeuchi Y, Abiko Y, Izumi Y (2012) Blue LED inhibits the growth of Porphyromonas gingivalis by suppressing the expression of genes associated with DNA replication and cell division. Lasers Surg Med. 44(10):856–864

    PubMed  Article  Google Scholar 

  44. Kreth J, Merritt J, Shi W, Qi F (2005) Competition and coexistence between Streptococcus mutans and Streptococcus sanguinis in the dental biofilm. J Bacteriol 187(21):7193–7203

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  45. Kuramitsu HK, He X, Lux R, Anderson MH, Shi W (2007) Interspecies interactions within oral microbial communities. Microbiol Mol Biol Rev 71(4):653–670

    CAS  PubMed  PubMed Central  Article  Google Scholar 

Download references

Funding

This work was partially supported by the United States-Israel Binational Science Foundation (BSF) grant (#2013445).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Osnat Feuerstein.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

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

Informed consent

Not applicable.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Vaknin, M., Steinberg, D., Featherstone, J.D. et al. Exposure of Streptococcus mutans and Streptococcus sanguinis to blue light in an oral biofilm model. Lasers Med Sci 35, 709–718 (2020). https://doi.org/10.1007/s10103-019-02903-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10103-019-02903-4

Keywords

  • Streptococcus mutans
  • Streptococcus sanguinis
  • Mixed biofilm
  • Blue light
  • Dental caries
  • Ecological balance