Metabolic activity of Streptococcus mutans biofilms and gene expression during exposure to xylitol and sucrose

International Journal of Oral Science

Volumn 6, Issue 4, 2014, Pages 195-204

  Decker, Eva Maria ^a   Klein, Christian ^a,b   Schwindt, Dimitri ^a   Von Ohle, Christiane ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Private Practice Zahngesundheit Waiblingen   (Germany)

Author keywords

3 ditolyl tetrazolium chloride; 5 cyano 2; biofilms; extracellular polysaccharides; gene expression; Streptococcus mutans; sucrose; viability; xylitol

Indexed keywords

1,3-ALPHA-D-GLUCAN SYNTHASE; 5-CYANO-2,3-DITOLYLTETRAZOLIUM; BACTERIAL POLYSACCHARIDE; CARIOGENIC AGENT; CULTURE MEDIUM; FLUORESCENT DYE; GLUCOSE; GLUCOSYLTRANSFERASE; GLUCOSYLTRANSFERASE C; SUCROSE; SWEETENING AGENT; TETRAZOLIUM; XYLITOL;

BACTERIAL LOAD; BIOFILM; BIOSYNTHESIS; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CULTURE MEDIUM; DIAGNOSTIC USE; DRUG EFFECTS; ENAMEL; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENOTYPE; HUMAN; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGICAL EXAMINATION; MICROBIOLOGY; STREPTOCOCCUS MUTANS; TIME; UPREGULATION;

BACTERIAL LOAD; BACTERIOLOGICAL TECHNIQUES; BIOFILMS; CARIOGENIC AGENTS; CULTURE MEDIA; DENTAL ENAMEL; FLUORESCENT DYES; GENE EXPRESSION REGULATION, BACTERIAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOTYPE; GLUCOSE; GLUCOSYLTRANSFERASES; HUMANS; MICROBIAL VIABILITY; MICROSCOPY, CONFOCAL; POLYSACCHARIDES, BACTERIAL; STREPTOCOCCUS MUTANS; SUCROSE; SWEETENING AGENTS; TETRAZOLIUM SALTS; TIME FACTORS; UP-REGULATION; XYLITOL;

EID: 84927167545     PISSN: 16742818     EISSN: 20493169     Source Type: Journal    
DOI: 10.1038/ijos.2014.38     Document Type: Article

References (56)

1. Ten Cate JM. Biofilms, a new approach to the microbiology of dental plaque. Odontology 2006; 94 (1): 1-9.
2. Hojo K, Nagaoka S, Ohshima T et al. Bacterial interactions in dental biofilm development. J Dent Res 2009; 88 (11): 982-990.
3. Stoodley P, Sauer K, Davies DGet al. Biofilms as complex differentiated communities. Annu Rev Microbiol 2002; 56: 187-209.
4. Forssten SD, Björklund M, Ouwehand AC. Streptococcus mutans, caries and simulation models. Nutrients 2010; 2 (3): 290-298.
5. Paes Leme AF, Koo H, BellatoCMet al. The role of sucrose in cariogenic dental biofilm formation-new insight. J Dent Res 2006; 85 (10): 878-887.
6. Narisawa N, Kawarai T, Suzuki N et al. Competence-dependent endogenous DNA rearrangement and uptake of extracellular DNA give a natural variant of Streptococcus mutans without biofilm formation. J Bacteriol 2011; 193 (19): 5147-5154.
7. Takahashi N, Nyvad B. Caries ecology revisited: microbial dynamics and the caries process. Caries Res 2008; 42 (6): 409-418.
8. Trahan L, Né ron S, Bareil M. Intracellular xylitol-phosphate hydrolysis and efflux of xylitol in Streptococcus sobrinus. Oral Microbiol Immunol 1991; 6 (1): 41-50.
9. Xiao J, Klein MI, Falsetta ML et al. The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. PLoS Pathog 2012; 8 (4): e1002623.
10. Klein MI, DeBaz L, Agidi S et al. Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during biofilm development. PLoS One 2010; 5 (10): e13478.
11. Rolerson E, Swick A, Newlon L et al. The SloR/Dlg metalloregulator modulates Streptococcus mutans virulence gene expression. J Bacteriol 2006; 188 (14): 5033-5044.
12. Senadheera MD, Guggenheim B, Spatafora GA et al. A VicRK signal transduction system in Streptococcus mutans affects gtfBCD, gbpB, and ftf expression, biofilm formation, and genetic competence development. J Bacteriol 2005; 187 (12): 4064-4076.
13. Shemesh M, Tam A, Steinberg D. Expression of biofilm-associated genes of Streptococcus mutans in response to glucose and sucrose. J Med Microbiol 2007; 56 (Pt 11): 1528-1535.
14. Shibata Y, Kawada M, Nakano Y et al. Identification and characterization of an autolysin-encoding gene of Streptococcus mutans. Infect Immun 2005; 73 (6): 3512-3520.
15. Banu LD, Conrads G, Rehrauer H et al. The Streptococcus mutans serine/threonine kinase, PknB, regulates competence development, bacteriocin production, and cell wall metabolism. Infect Immun 2010; 78 (5): 2209-2220.
16. Shemesh M, Tam A, Kott-Gutkowski M et al. DNA-microarrays identification of Streptococcus mutans genes associated with biofilm thickness. BMC Microbiol 2008; 8: 236.
17. Sztajer H, Lemme A, Vilchez R et al. Autoinducer-2-regulated genes in Streptococcus mutans UA159 and global metabolic effect of the luxS mutation. J Bacteriol 2008; 190 (1): 401-415.
18. ShemeshM, Tam A, FeldmanMet al. 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 2006; 341 (12): 2090-2097.
19. Gong Y, Tian XL, Sutherland T et al. Global transcriptional analysis of acid-inducible genes in Streptococcus mutans: multiple two-component systems involved in acid adaptation. Microbiology 2009; 155 (Pt 10): 3322-3332.
20. Mä kinen KK. Sugar alcohol sweeteners as alternatives to sugar with special consideration of xylitol. Med Princ Pract 2011; 20 (4): 303-320.
21. Tanzer JM. Xylitol chewing gum and dental caries. Int Dent J 1995; 45 (1 Suppl 1): 65-76.
22. Trahan L. Xylitol: a review of its action on mutans streptococci and dental plaque-its clinical significance. Int Dent J 1995; 45 (1 Suppl 1): 77-92.
23. Giertsen E, Arthur RA, Guggenheim B. Effects of xylitol on survival of mutans streptococci in mixed-six-species in vitro biofilms modelling supragingival plaque. Caries Res 2011; 45 (1): 31-39.
24. Scheie AA, Fejerskov O, Danielsen B. The effects of xylitol-containing chewing gums on dental plaque and acidogenic potential. J Dent Res 1998; 77 (7): 1547-1552.
25. Anderson SA, Sissons CH, Coleman MJ et al. Application of carbon source utilization patterns to measure the metabolic similarity of complex dental plaque biofilm microcosms. Appl Environ Microbiol 2002; 68 (11): 5779-5783.
26. Decker EM, Weiger R, von Ohle C et al. Susceptibility of planktonic versus attached Streptococcus sanguinis cells to chlorhexidine. Clin Oral Investig 2003; 7 (2): 98-102.
27. Willems G, Lambrechts P, BraemMet al. The surface roughness of enamel-to-enamel contact areas compared with the intrinsic roughness of dental resin composites. J Dent Res 1991; 70 (9): 1299-1305.
28. Decker EM. The ability of direct fluorescence-based, two-colour assays to detect different physiological states of oral streptococci. Lett Appl Microbiol 2001; 33 (3): 188-192.
29. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 2001; 25 (4): 402-408.
30. Aires CP, Tabchoury CP, del bel Cury AA et al. Effect of sucrose concentration on dental biofilm formed in situ and on enamel demineralization. Caries Res 2006; 40 (1): 28-32.
31. Zhu M, Takenaka S, SatoMet al. Influence of starvation and biofilm formation on acid resistance of Streptococcus mutans. Oral Microbiol Immunol 2001; 16 (1): 24-27.
32. Marttinen AM, Ruas-Madiedo P, Hidalgo-Cantabrana C et al. Effects of xylitol on xylitol-sensitive versus xylitol-resistant Streptococcus mutans strains in a threespecies in vitro biofilm. Curr Microbiol 2012; 65 (3): 237-243.
33. Badet C, Furiga A, Thébaud N. Effect of xylitol on an in vitro model of oral biofilm. Oral Health Prev Dent 2008; 6 (4): 337-341.
34. Söderling EM, Ekman TC, Taipale TJ. Growth inhibition of Streptococcus mutans with low xylitol concentrations. Curr Microbiol 2008; 56 (4): 382-385.
35. Lif Holgerson P, Stecksén-Blicks C, Sjöström I et al. Xylitol concentration in saliva and dental plaque after use of various xylitol-containing products. Caries Res 2006; 40 (5): 393-397.
36. Tapiainen T, Renko M, Kontiokari T et al. Xylitol concentrations in the saliva of children after chewing xylitol gum or consuming a xylitol mixture. Eur J Clin Microbiol Infect Dis 2002; 21 (1): 53-55.
37. Hanada N, Kuramitsu HK. Isolation and characterization of the Streptococcus mutans gtfC gene, coding for synthesis of both soluble and insoluble glucans. Infect Immun 1988; 56 (8): 1999-2005.
38. Nakano K, Nomura R, Nemoto H et al. Protein antigen in serotype k Streptococcus mutans clinical isolates. J Dent Res 2008; 87 (10): 964-968.
39. Trahan L, Bareil M, Gauthier L et al. Transport and phosphorylation of xylitol by a fructose phosphotransferase system in Streptococcus mutans. Caries Res 1985; 19 (1): 53-63.
40. Assev S, Rölla G. Further studies on the growth inhibition of Streptococcus mutans OMZ 176 by xylitol. Acta Pathol Microbiol Immunol Scand B 1986; 94 (2): 97-102.
41. Lee YE, Choi YH, Jeong SH et al. Morphological changes in Streptococcus mutans after chewing gum containing xylitol for twelve months. Curr Microbiol 2009; 58 (4): 332-337.
42. van Loveren C. Sugar alcohols: what is the evidence for caries-preventive and cariestherapeutic effects? Caries Res 2004; 38 (3): 286-293.
43. Tapiainen T, Kontiokari T, Sammalkivi L et al. Effect of xylitol on growth of Streptococcus pneumoniae in the presence of fructose and sorbitol. Antimicrob Agents Chemother 2001; 45 (1): 166-169.
44. Kurola P, Tapiainen T, Sevander J et al. Effect of xylitol and other carbon sources on Streptococcus pneumoniae biofilm formation and gene expression in vitro. APMIS 2011; 119 (2): 135-142.
45. Pal A, Paul AK. Optimization of cultural conditions for production of extracellular polymeric substances (EPS) by serpentine rhizobacterium Cupriavidus pauculus KPS 201. J Polym 2013; 2013: 692374.
46. Sims IM, Frese SA, Walter J et al. Structure and functions of exopolysaccharide produced by gut commensal Lactobacillus reuteri 100-23. ISME J 2011; 5 (7): 1115-1124.
47. Decker EM, Dietrich I, Klein C et al. Dynamic production of soluble extracellular polysaccharides by Streptococcus mutans. Int J Dent 2011; 2011: 435830.
48. Bowen WH. Do we need to be concerned about dental caries in the coming millennium? Crit Rev Oral Biol Med 2002; 13 (2): 126-131.
49. Pecharki GD, Cury JA, Paes Leme AF et al. Effect of sucrose containing iron (II) on dental biofilm and enamel demineralization in situ. Caries Res 2005; 39 (2): 123-129.
50. Kreth J, Zhu L, Merritt J et al. Role of sucrose in the fitness of Streptococcus mutans. Oral Microbiol Immunol 2008; 23 (3): 213-219.
51. Yamashita Y, Bowen WH, Burne RA et al. Role of the Streptococcus mutans gtf genes in caries induction in the specific-pathogen-free rat model. Infect Immun 1993; 61 (9): 3811-3817.
52. TsumoriH, Kuramitsu H. The role of the Streptococcus mutans glucosyltransferases in the sucrose-dependent attachment to smooth surfaces: essential role of the GtfC enzyme. Oral Microbiol Immunol 1997; 12 (5): 274-280.
53. Renye JA Jr, Piggot PJ, Daneo-Moore L et al. Persistence of Streptococcus mutans in stationary-phase batch cultures and biofilms. Appl Environ Microbiol 2004; 70 (10): 6181-6187.
54. Koo H, Xiao J, Klein MI et al. Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J Bacteriol 2010; 192 (12): 3024-3032.
55. Gu H, Fan D, Gao J et al. Effect of ZnCl2 on plaque growth and biofilm vitality. Arch Oral Biol 2012; 57 (4): 369-375.
56. Zaura-Arite E, van Marle J, ten Cate JM. Conofocal microscopy study of undisturbed and chlorhexidine-treated dental biofilm. J Dent Res 2001; 80 (5): 1436-1440.