Abstract
We investigated the effect of xylitol or/and funoran on biofilm formation by Streptococcus mutans, one of cariogenic bacteria, on the surfaces coated and non-coated with saliva. Effects of xylitol and/or funoran were observed on biofilm formation of S. mutans in non-coated and salivary components-coated polystyrene microtiter 96-well plates (s-plate) and flow cell system. Xylitol did not strongly affect biofilm formation of S. mutans UA159 on non-coated and s-plates and, however, changed the quality of the biofilm on the cells in a flow cell system. Funoran had effects on biofilm formation, and the combination of xylitol and funoran strongly inhibited S. mutans biofilm formation on non-coated plates. In particular, funoran had inactivation effects on membrane vesicles (MVs) and inhibited MV-dependent biofilm formation of S. mutans on non-coated plate surfaces but not on the s-plate. These findings suggest that the combination of xylitol and funoran might be useful to remove the oral biofilm formation in elderly individuals with decreased saliva production. This result suggests that the synergistic effect of funoran and xylitol might be useful for the prevention of biofilm-associated diseases such as dental caries in saliva-decreased patients such as elderly patients.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahn SJ, Ahn SJ, Wen ZT et al (2008) Characteristics of biofilm formation by Streptococcus mutans in the presence of saliva. Infect Immun 76:4259–4268. https://doi.org/10.1128/IAI.00422-08
Arianto YKE, Prawirowinoto ST, Asada S, Saeki Y (2016) Combination concentration effects of calcium hydrogenphosphate on human enamel remineralization by xylitol and funoran. J Int Dent Med Res 9:189–194
Banas JA (2004) Virulence properties of Streptococcus mutans. Front Biosci 9:1267–1277. https://doi.org/10.2741/1305
Ben-Aryeh H, Miron D, Szargel R, Gutman D (1984) Clinical science whole-saliva secretion rates in old and young healthy subjects. J Dent Res 63:1147–1148. https://doi.org/10.1177/00220345840630091001
Bowen WH, Koo H (2011) Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular, matrix formation of cariogenic biofilms. Caries Res 45:69–86. https://doi.org/10.1159/000324598
Brambilla E, Ionescu AC, Cazzaniga G, Ottobelli M, Samaranayake LP (2016) Levorotatory carbohydrates and xylitol subdue Streptococcus mutans and Candida albicans adhesion and biofilm formation. J Basic Microbiol 56:480–492. https://doi.org/10.1002/jobm.201500329
Brown L, Wolf JM, Prados-Rosales R, Casadevall A (2015) Through the wall: extracellular vesicles in Gram-positive bacteria, mycobacteria and fungi. Nat Rev Microbiol 13:620–630. https://doi.org/10.1038/nrmicro3480
Burt B (2006) The use of sorbitol- and xylitol-sweetened chewing gum in caries control. J Am Dent Assoc 137:190–196. https://doi.org/10.14219/jada.archive.2006.0144
Carlucci MJ, Pujol CA, Ciancia M, Noseda MD et al (1997) Antiherpetic and anticoagulant properties of carrageenans from the red seaweed Gigartina skottsbergii and their cyclized derivatives: correlation between structure and biological activity. Int J Biol Macromol 20:97–105. https://doi.org/10.1016/s0141-8130(96)01145-2
Decker EM, Klein C, Schwindt D, Ohle CV (2014) Metabolic activity of Streptococcus mutans biofilms and gene expression during exposure to xylitol and sucrose. Int J Oral Sci 6:195–204. https://doi.org/10.1038/ijos.2014.38
Donachie MA, Walls AW (1995) Assessment of tooth wear in an ageing population. J Dent 23:157–164. https://doi.org/10.1016/0300-5712(95)93573-k
Ericson T, Rundegren J (1983) Characterization of a salivary agglutinin reacting with a serotype c strain of Streptococcus mutans. Eur J Biochem 133:255–261. https://doi.org/10.1111/j.1432-1033.1983.tb07456.x
Farias WR, Valente AP, Pereira MS, Mourão PA (2000) Structure and anticoagulant activity of sulfated galactans. Isolation of a unique sulfated galactan from the red algae Botryocladia occidentalis and comparison of its anticoagulant action with that of sulfated galactans from invertebrates. J Biol Chem 275:29299–29307. https://doi.org/10.1074/jbc.M002422200
Feng G, Klein MI, Gregoire S, Singh AP, Vorsa N, Koo H (2013) The specific degree-of-polymerization of A-type proanthocyanidin oligomers impacts Streptococcus mutans glucan-mediated adhesion and transcriptome responses within biofilms. Biofouling 29:629–640. https://doi.org/10.1080/08927014.2013.794456
Fox PC, Bowman SJ, Segal B, Vivino FB, Murukutla N, Choueiri K, Ogale S, Mclean L (2008) Oral involvement in primary Sjögren syndrome. J Am Dent Assoc 139:1592–1601. https://doi.org/10.14219/jada.archive.2008.0101
Gerritsen AE, Allen PF, Witter DJ, Bronkhorst EM, Creugers NH (2010) Tooth loss and oral health-related quality of life: a systematic review and meta-analysis. Health Qual Life Outcomes 8:126. https://doi.org/10.1186/1477-7525-8-126
Giertsen E, Arthur RA, Guggenheim B (2011) Effects of xylitol on survival of mutans Streptococci in mixed-six-species in vitro biofilms modelling supragingival plaque. Caries Res 45:31–39. https://doi.org/10.1159/000322646
Grenby TH, Phillips A, Mistry M (1989) Studies of the dental properties of lactitol compared with five other bulk sweeteners in vitro. Caries Res 23:315–319. https://doi.org/10.1159/000261199
Guan C, Che F, Zhou H, Li Y, Chu J (2020) Effect of rubusoside, a natural sucrose substitute, on Streptococcus mutans biofilm cariogenic potential and virulence gene expression in vitro. Appl Environ Microbiol 86:e01012–20. https://doi.org/10.1128/AEM.01012-20
Hajishengallis E, Parsaei Y, Klein MI, Koo H (2017) Advances in the microbial etiology and pathogenesis of early childhood caries. Mol Oral Microbiol 32:24–34. https://doi.org/10.1111/omi.12152
Haresaku S, Hanioka T, Tsutsui A, Yamamoto M, Chou T, Gunjishima Y (2007) Long-term effect of xylitol gum use on mutans streptococci in adults. Caries Res 41:198–203. https://doi.org/10.1159/000099318
Holt RG, Abiko Y, Saito S, Smorawinska M, Hansen JB, Curtiss R III (1982) Streptococcus mutans genes that code for extracellular proteins in Escherichia coli K-12. Infect Immun 38:147–156. https://doi.org/10.1128/iai.38.1.147-156.1982
Inagaki S, Saeki Y, Ishihara K (2011) Funoran-containing xylitol gum and tablets inhibit adherence of oral streptococci. J Oral Biosci 53:82–86
Isokangas P, Alanen P, Tiekso J, Makinen KK (1988) Xylitol chewing gum in caries prevention: a field study in children. J Am Dent Assoc 117:315–320
Klein MI, Xiao J, Lu B, Delahunty CM, Yates JR 3rd, Koo H (2012) Streptococcus mutans protein synthesis during mixed-species biofilm development by high-throughput quantitative proteomics. PLoS ONE 7:e45795. https://doi.org/10.1371/journal.pone.0045795
Knuuttila ML, Mäkinen K (1975) Effect of xylitol on the growth and metabolism of Streptococcus mutans. Caries Res 9:177–189. https://doi.org/10.1159/000260156
Lee SH, Choi BH, Kim YJ (2012) The cariogenic characters of xylitol-resistant and xylitol-sensitive Streptococcus mutans in biofilm formation with salivary bacteria. Arch Oral Biol 57:697–703. https://doi.org/10.1016/j.archoralbio.2011.12.001
Liao S, Klein MI, Heim KP, Fan Y et al (2014) 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 196:2355–2366. https://doi.org/10.1128/JB.01493-14
Loesche WJ (1986) Role of Streptococcus mutans in human dental decay. Microbiol Rev 50:353–380. https://doi.org/10.1128/mr.50.4.353-380.1986
Malamud D, Appelbaum B, Kline R, Golub EE (1981) Bacterial aggregating activity in human saliva: comparisons of bacterial species and strains. Infect Immun 31:1003–1006. https://doi.org/10.1128/iai.31.3.1003-1006.1981
Miake Y, Saeki Y, Takahashi M, Yanagisawa T (2003) Remineralization effects of xylitol on demineralized enamel. J Electron Microsc 52:471–476. https://doi.org/10.1093/jmicro/52.5.471
Milgrom P, Ly KA, Roberts MC, Rothen M, Mueller G, Yamaguchi DK (2006) Mutans streptococci dose response to xylitol chewing gum. J Dent Res 85:177–181. https://doi.org/10.1177/154405910608500212
Miyasawa-Hori H, Aizawa S, Takahashi N (2006) Difference in the xylitol sensitivity of acid production among Streptococcus mutans strains and the biochemical mechanism. Oral Microbiol Immunol 21:201–205. https://doi.org/10.1111/j.1399-302X.2006.00273.x
Motegi M, Takagi Y, Yonezawa H, Hanada N et al (2006) Assessment of genes associated with Streptococcus mutans biofilm morphology. Appl Environ Microbiol 72:6277–6287. https://doi.org/10.1128/AEM.00614-06
Najera MP, Al-Hashimi I, Plemons JM, Rivera-Hidalgo F (1997) Prevalence of periodontal disease in patients with Sjögren’s syndrome. Oral Sug Oral Med Oral Pathol 83:453–457. https://doi.org/10.1016/s1079-2104(97)90144-x
Nakamura T, Iwabuchi Y, Hirayama S, Narisawa N et al (2020) Roles of membrane vesicles from Streptococcus mutans for the induction of antibodies to glucosyltransferase in mucosal immunity. Microb Pathog 15:104260. https://doi.org/10.1016/j.micpath.2020.104260
Nishino T, Aizu Y, Nagumo T (1991) Antithrombin activity of a fucan sulfate from the brown seaweed Ecklonia Kurome. Thromb Res 62:765–773. https://doi.org/10.1016/0049-3848(91)90380-f
Okahashi N, Sasakawa C, Yoshikawa M, Hamada S, Koga T (1989) Cloning of a surface protein antigen gene from serotype c Streptococcus mutans. Mol Microbiol 3:221–228. https://doi.org/10.1111/j.1365-2958.1989.tb01811.x
Okamura K, Katsuragi H, Saito K (2001) Effect of xylitol on growth and water-insoluble glucan formation of mutans streptococci. Oral Therap Pharmacol 20:199–208
Ooshima T, Matsumura M, Hoshino T, Kawabata S et al (2001) Contributions of three glucosyltransferases to sucrose-dependent adherence of Streptococcus mutans. J Dent Res 80:1672–1677. https://doi.org/10.1177/00220345010800071401
Orench-Rivera N, Kuehn MJ (2016) Environmentally controlled bacterial vesicle-mediated export. Cell Microbiol 18:1525–1536. https://doi.org/10.1111/cmi.12676
Pereira MS, Mulloy B, Mourão PA (1999) Structure and anticoagulant activity of sulfated fucans. Comparison between the regular, repetitive, and linear fucans from echinoderms with the more heterogeneous and branched polymers from brown algae. J Biol Chem 274:7656–7667. https://doi.org/10.1074/jbc.274.12.7656
Russell RRB (1979) Wall-associated protein antigens of Streptococcus mutans. J Gen Microbiol 114:109–115. https://doi.org/10.1099/00221287-114-1-109
Saeki Y (1994) Effect of seaweed extracts on Streptococcus sobrinus adsorption to saliva-coated hydroxyapatite. Bull Tokyo Dent Coll 35:9–15
Saeki Y, Kato T, Naito Y, Takazoe I, Okuda K (1996a) Inhibitory effects of funoran on the adherence and colonization of mutans streptococci. Caries Res 30:119–125. https://doi.org/10.1159/000262147
Saeki Y, Kato T, Okuda K (1996b) Inhibitory effects of funoran on the adherence and colonization of oral bacteria. Bull Tokyo Dent Coll 37:77–92. https://doi.org/10.1159/000262147
Sato S, Yoshinuma N, Ito K, Tokumoto T, Takiguchi T, Suzuki Y, Murai S (1998) The inhibitory effect of funoran and eucalyptus extract-containing chewing gum on plaque formation. J Oral Sci 40:115–117. https://doi.org/10.2334/josnusd.40.115
Senpuku H, Nakamura T, Iwabuchi Y, Hirayama S et al (2019) Effects of complex DNA and MVs with GTF extracted from Streptococcus mutans on the oral biofilm. Molecules 24:3131. https://doi.org/10.3390/molecules24173131
Söderling E, Isokangas P, Tenovuo J, Mustakallio S, Mäkinen KK (1991) Long-term xylitol consumption and mutans streptococci in plaque and saliva. Caries Res 25:153–157. https://doi.org/10.1159/000261359
Suzuki Y, Nagasawa R, Senpuku H (2017) Inhibiting effects of fructanase on competence-stimulating peptide-dependent quorum sensing system in Streptococcus mutans. J Infect Chemother 23:634–641. https://doi.org/10.1016/j.jiac.2017.06.006
Synnöve A, Gunnar R (1986) Further Studies on the growth inhibition of Streptococcus mutans OMZ 176 by xylitol. Acta Pathol Microbiol Immunol Scand Ser B Microbiol 94B:97–102
Takano R, Hayashi S, Hara S, Hirase S (1995) Funoran from the red seaweed, Gloiopeltis complanata: polysaccharides with sulphated agarose structure and their precursor structure. Crbohydrate Polm 27:305–311
Takano R, Iwane-Sakata H, Hayashi K, Hara S, Hirase S (1998) Concurrence of agaroid and carrageenan chains in funoran from the red seaweed Gloiopeltis furcata post. et ruprecht (cryptonemials, rhodophyta). Carbohydr Polm 35:81–87
Tam K, Kinsinger N, Ayala P, Qi F, Shi W, Myung NV (2007) Real-time monitoring of Streptococcus mutans biofilm formation using a quartz crystal microbalance. Caries Res 41:474–483. https://doi.org/10.1159/000108321
Thaweboon S, Nakornchai S, Miyake Y, Yanagisawa T et al (2009) Remineralization of enamel subsurface lesions by xylitol chewing gum containing funoran and calcium hydrogenphosphate. Southeast Asian J Trop Med Public Health 40:345–353
Tollefsen DM, Majerus DW, Blank MK (1982) Heparin cofactor II. Purification and properties of a heparin-dependent inhibitor of thrombin in human plasma. J Biol Chem 257:2162–2169
Tollefsen DM, Pestka CA, Monafo WJ (1983) Activation of heparin cofactor II by dermatan sulfate. J Biol Chem 258:6713–6716
Toyofuku M, Nomura N, Eberl L (2019) Types and origins of bacterial membrane vesicles. Nat Rev Microbiol 17:13–24. https://doi.org/10.1038/s41579-018-0112-2
Trahan L, Bareil M, Gauthier L, Vadeboncoeur C (1985) Transport and phosphorylation of xylitol by a fructose phosphotransferase system in Streptococcus mutans. Caries Res 19:53–63. https://doi.org/10.1159/000260829
Zhu P, Masuda Y, Kumoto K (2004) The effect of surface charge on hydroxyapatite nucleation. Biomaterials 25:3915–3921. https://doi.org/10.1016/j.biomaterials.2003.10.022
Acknowledgements
The authors thank Taisuke Fujibayashi, Moriyuki Nakamura, Abdus Salam, Ryoma Nakao, and Yoji Saeki for their technical support, helpful discussions, and advice.
Funding
This work was supported in part by Grants-in-Aid for the Development of Scientific Research (16K11537 and 20K10286) from the Ministry of Education, Culture, Sports, Science and Technology (MEXT), and the Re-emerging Infectious Diseases from the Japan Agency for Medical Research and Development, AMED (40105502).
Author information
Authors and Affiliations
Contributions
TN, HY, and HS contributed to the data collection and data acquisition. HS, TN, TK, and NN contributed to the manuscript review. HS and HY contributed to the concept, design, and literature search. HS contributed to the fund acquisition, manuscript preparation, and manuscript editing. All the authors approved the final version of the manuscript for publication.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interests.
Additional information
Communicated by Erko Stackebrandt.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Nakamura, T., Yonezawa, H., Kawarai, T. et al. Inhibitory effect of the combination of xylitol and funoran on Streptococcus mutans biofilm formation on the uncoated surface. Arch Microbiol 204, 723 (2022). https://doi.org/10.1007/s00203-022-03299-6
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00203-022-03299-6