Food-grade Lacticaseibacillus paracasei postbiotics suppress oral Streptococcus mutans biofilm formation and cariogenicity

1. Wen, P. Y. F., Chen, M. X., Zhong, Y. J., Dong, Q. Q. & Wong, H. M. Global burden and inequality of dental caries, 1990 to 2019. J. Dent. Res. 101, 392–399 (2022).

   Google Scholar 

2. Hajishengallis, E., Parsaei, Y., Klein, M. I. & Koo, H. Advances in the microbial etiology and pathogenesis of early childhood caries. Mol. Oral. Microbiol. 32, 24–34 (2017).

   Google Scholar 

3. Gong, Y. et al. Global transcriptional analysis of acid-inducible genes in Streptococcus mutans: multiple two-component systems involved in acid adaptation. Microbiology 155, 3322–3332 (2009).

   Google Scholar 

4. Peres, M. A. et al. Oral diseases: a global public health challenge. Lancet 394, 249–260 (2019).

   Google Scholar 

5. Luo, S. C. et al. How probiotics, prebiotics, synbiotics, and postbiotics prevent dental caries: an oral microbiota perspective. npj Biofilms Microbiomes 10, 1–15 (2024).

   Google Scholar 

6. Baker, J. L. et al. Deep metagenomics examines the oral microbiome during dental caries, revealing novel taxa and co-occurrences with host molecules. Genome Res. 31, 64–74 (2021).

   Google Scholar 

7. Legenova, K. & Bujdakova, H. The role of Streptococcus mutans in the oral biofilm. Epidemiol. Mikrobiol. Imunol. 64, 179–187 (2015).

   Google Scholar 

8. Philip, N., Suneja, B. & Walsh, L. J. Ecological approaches to dental caries prevention: paradigm shift or shibboleth. Caries Res. 52, 153–165 (2018).

   Google Scholar 

9. Yu, O. Y., Lam, W. Y., Wong, A. W., Duangthip, D. & Chu, C. H. Nonrestorative management of dental caries. Dent. J. 9, 121 (2021).

   Google Scholar 

10. Inchingolo, A. D. et al. Oralbiotica/oralbiotics: the impact of oral microbiota on dental health and demineralization: a systematic review of the literature. Child. -Basel 9, 1014 (2022).

    Google Scholar 

11. Salminen, S. et al. The International Scientific Association of Probiotics and Prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics. Nat. Rev. Gastroenterol. Hepatol. 18, 649–667 (2021).

    Google Scholar 

12. Moradi, M. et al. Postbiotics produced by lactic acid bacteria: the next frontier in food safety. Compr. Rev. Food Sci. Food Saf. 19, 3390–3415 (2020).

    Google Scholar 

13. Lin, C.-W. et al. Impact of the food grade heat-killed probiotic and postbiotic oral lozenges in oral hygiene. Aging 14, 2221–2238 (2022).

    Google Scholar 

14. Nataraj, B. H., Ramesh, C. & Mallappa, R. H. Characterization of biosurfactants derived from probiotic lactic acid bacteria against methicillin-resistant and sensitive Staphylococcus aureus isolates. LWT-Food Sci. Technol. 151, 112195 (2021).

    Google Scholar 

15. Zhou, K. et al. Mode of action of pentocin 31-1: an antilisteria bacteriocin produced by Lactobacillus pentosus from Chinese traditional ham. Food Control 19, 817–822 (2008).

    Google Scholar 

16. Jin, X. et al. Sensitive bacterial Vm sensors revealed the excitability of bacterial Vm and its role in antibiotic tolerance. Proc. Natl. Acad. Sci. USA 120, e2208348120 (2023).

    Google Scholar 

17. Kaplan, C. W. et al. Selective membrane disruption: mode of action of C16G2, a specifically targeted antimicrobial peptide. Antimicrob. Agents Chemother. 55, 3446–3452 (2011).

    Google Scholar 

18. Haidinger, W., Szostak, M. P., Jechlinger, W. & Lubitz, W. Online monitoring of Escherichia coli ghost production. Appl. Environ. Microbiol. 69, 468–474 (2003).

    Google Scholar 

19. Jang, H. J., Kim, J. H., Lee, N.-K. & Paik, H.-D. Inhibitory effects of Lactobacillus brevis KU15153 against Streptococcus mutans KCTC 5316 causing dental caries. Microb. Pathog. 157, 104938–79 (2021).

    Google Scholar 

20. Hori, K. & Matsumoto, S. Bacterial adhesion: From mechanism to control. Biochem. Eng. J. 48, 424–434 (2010).

    Google Scholar 

21. Luo, Y. P., Li, Y. J. & Yan, G. A. A review on the surface hydrophobicity of bacteria and algae and its ecological significance. Trans. Oceanol. Limnol. 4, 71–79 (1997).

    Google Scholar 

22. Tahmourespour, A., Salehi, R. & Kasra Kermanshahi, R. Lactobacillus acidophilus-derived biosurfactant effect on gtfB and gtfC expression level in Streptococcus mutans biofilm cells. Braz. J. Microbiol. 42, 330–339 (2011).

    Google Scholar 

23. Lin, T. H., Lin, C. H. & Pan, T. M. The implication of probiotics in the prevention of dental caries. Appl. Microbiol. Biotechnol. 102, 577–586 (2018).

    Google Scholar 

24. Wasfi, R., Abd El-Rahman, O. A., Zafer, M. M. & Ashour, H. M. Probiotic Lactobacillus sp. inhibit growth, biofilm formation and gene expression of caries-inducing Streptococcus mutans. J. Cell. Mol. Med. 22, 1972–1983 (2018).

    Google Scholar 

25. Vecino, X. et al. Vineyard pruning waste as an alternative carbon source to produce novel biosurfactants by Lactobacillus paracasei. J. Ind. Eng. Chem. 55, 40–49 (2017).

    Google Scholar 

26. Lim, H.-S., Yeu, J.-E., Hong, S.-P. & Kang, M.-S. Characterization of antibacterial cell-free supernatant from oral care probiotic weissella cibaria, CMU. Molecules 23, 1984 (2018).

    Google Scholar 

27. van Swaaij, B. W. M., Slot, D. E., Van der Weijden, G. A., Timmerman, M. F. & Ruben, J. Fluoride, pH value, and titratable acidity of commercially available mouthwashes. Int. Dent. J. 72, 260–267 (2023).

    Google Scholar 

28. Li, Y. & Zheng, J. Comparative study on the mechanical properties of human tooth enamel and synthetic hydroxyapatite. Lubr. Eng. 36, 43–46+67 (2011).

    Google Scholar 

29. Liu, Y. et al. Topical delivery of low-cost protein drug candidates made in chloroplasts for biofilm disruption and uptake by oral epithelial cells. Biomaterials 105, 156–166 (2016).

    Google Scholar 

30. Schneider-Rayman, M., Steinberg, D., Sionov, R. V., Friedman, M. & Shalish, M. Effect of epigallocatechin gallate on dental biofilm of Streptococcus mutans: an in vitro study. BMC Oral Health 21, 447 (2021).

    Google Scholar 

31. Zhang, J. et al. Inactivation of glutamate racemase (MurI) eliminates virulence in Streptococcus mutans. Microbiol. Res. 186–187, 1–8 (2016).

    Google Scholar 

32. Banas, J. A. Virulence properties of Streptococcus mutans. Front. Biosci. -Landmark 9, 1267–1277 (2004).

    Google Scholar 

33. Li, Z., Xiang, Z., Zeng, J., Li, Y. & Li, J. A GntR family transcription factor in Streptococcus mutans regulates biofilm formation and expression of multiple sugar transporter genes. Front. Microbiol. 9, 3224 (2019).

    Google Scholar 

34. Lin, Y., Chen, J., Zhou, X. & Li, Y. Inhibition of Streptococcus mutans biofilm formation by strategies targeting the metabolism of exopolysaccharides. Crit. Rev. Microbiol. 47, 667–677 (2021).

    Google Scholar 

35. Banas, J. A., Fountain, T. L., Mazurkiewicz, J. E., Sun, K. & Vickerman, M. M. Streptococcus mutans glucan-binding protein-A affects Streptococcus gordonii biofilm architecture. FEMS Microbiol. Lett. 267, 80–88 (2007).

    Google Scholar 

36. Wang, C., van der Mei, H. C., Busscher, H. J. & Ren, Y. Streptococcus mutans adhesion force sensing in multi-species oral biofilms. npj Biofilms Microbiomes 6, 1–9 (2020).

    Google Scholar 

37. Hasan, S., Singh, K., Danisuddin, M., Verma, P. K. & Khan, A. U. Inhibition of major virulence pathways of Streptococcus mutans by quercitrin and deoxynojirimycin: a synergistic approach of infection control. Plos One 9, e91736 (2014).

    Google Scholar 

38. Wang, Y. et al. Antimicrobial peptide GH12 suppresses cariogenic virulence factors of Streptococcus mutans. J. Oral. Microbiol. 10, 1442089 (2018).

    Google Scholar 

39. Zeng, L. & Burne, R. A. Comprehensive mutational analysis of sucrose-metabolizing pathways in Streptococcus mutans reveals novel roles for the sucrose phosphotransferase system permease. J. Bacteriol. 195, 833–843 (2013).

    Google Scholar 

40. Liu, Y. & Burne, R. A. Multiple two-component systems of Streptococcus mutans regulate agmatine deiminase gene expression and stress tolerance. J. Bacteriol. 191, 7363–7366 (2009).

    Google Scholar 

41. Linares, D. M. et al. The putrescine biosynthesis pathway in Lactococcus lactis is transcriptionally regulated by carbon catabolic repression, mediated by CcpA. Int. J. Food Microbiol. 165, 43–50 (2013).

    Google Scholar 

42. Kuhnert, W. L. & Quivey, R. G. Genetic and biochemical characterization of the F-ATPase operon from Streptococcus sanguis 10904. J. Bacteriol. 185, 1525–1533 (2003).

    Google Scholar 

43. Li, Y. H. & Tian, X. L. Quorum sensing and bacterial social interactions in biofilms. Sensors 12, 2519–2538 (2012).

    Google Scholar 

44. Li, Y. H. et al. A quorum-sensing signaling system essential for genetic competence in Streptococcus mutans is involved in biofilm formation. J. Bacteriol. 184, 2699–2708 (2002).

    Google Scholar 

45. Senadheera, M. D. et al. A vicRX signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J. Bacteriol. 187, 4064–4076 (2005).

    Google Scholar 

46. Ahmed, A. et al. Effect of Lactobacillus species on Streptococcus mutans Biofilm formation. Pak. J. Pharm. Sci. 27, 1523–1528 (2014).

    Google Scholar 

47. Yan, J. et al. vicR overexpression in Streptococcus mutans causes aggregation and affects interspecies competition. Mol. Oral. Microbiol. 38, 224–236 (2023).

    Google Scholar 

48. Suzuki, Y., Nagasawa, R. & Senpuku, H. Inhibiting effects of fructanase on competence-stimulating peptide-dependent quorum sensing system in Streptococcus mutans. J. Infect. Chemother. 23, 634–641 (2017).

    Google Scholar 

49. Wu, C. et al. Regulation of ciaXRH operon expression and identification of the CiaR regulon in Streptococcus mutans. J. Bacteriol. 192, 4669–4679 (2010).

    Google Scholar 

50. He, X. et al. The cia operon of Streptococcus mutans encodes a unique component required for calcium-mediated autoregulation. Mol. Microbiol. 70, 112–126 (2008).

    Google Scholar 

51. Zhu, B. et al. ciaR impacts biofilm formation by regulating an arginine biosynthesis pathway in Streptococcus sanguinis SK36. Sci. Rep. 7, 17183 (2017).

    Google Scholar 

52. Heimisdottir, L. H. et al. Metabolomics insights in early childhood caries. J. Dent. Res. 100, 615–622 (2021).

    Google Scholar 

53. Kreider, R. B. & Stout, J. R. Creatine in health and disease. Nutrients 13, 447 (2021).

    Google Scholar 

54. Falsetta, M. L. et al. Novel antibiofilm chemotherapy targets exopolysaccharide synthesis and stress tolerance in Streptococcus mutans to modulate virulence expression in vivo. Antimicrob. Agents Chemother. 56, 6201–6211 (2012).

    Google Scholar 

55. Copley, T. R., Aliferis, K. A., Kliebenstein, D. J. & Jabaji, S. H. An integrated RNAseq-¹H NMR metabolomics approach to understand soybean primary metabolism regulation in response to Rhizoctonia foliar blight disease. BMC Plant Biol. 17, 84 (2017).

    Google Scholar 

Download references