Efficiency of Bacillus subtilis metabolism of sugar alcohols governs its probiotic effect against cariogenic Streptococcus mutans

References

• Hong HA, Duc LH, Cutting SM. The use of bacterial spore formers as probiotics. FEMS Microbiol Rev. 2005;29(4):813–835.
   PubMed Web of Science ®Google Scholar
• Cutting SM. Bacillus probiotics. Food Microbiol. 2011;28(2):214–220.
   PubMed Web of Science ®Google Scholar
• Mazza P. The use of Bacillus subtilis as an antidiarrhoeal microorganism. Boll Chim Farm. 1994;133(1):3–18.
   PubMedGoogle Scholar
• Hong H, Huang JM, Khaneja R, et al. The safety of Bacillus subtilis and Bacillus indicus as food probiotics. J Appl Microbiol. 2008;105(2):510–520.
   PubMed Web of Science ®Google Scholar
• Spinosa MR, Braccini T, Ricca E, et al. On the fate of ingested Bacillus spores. Res Microbiol. 2000;151(5):361–368.
   PubMed Web of Science ®Google Scholar
• Sanders M, Morelli L, Tompkins T. Sporeformers as human probiotics: Bacillus, Sporolactobacillus, and Brevibacillus. Comp Rev Food Sci Food Safety. 2003;2(3):101–110.
   PubMedGoogle Scholar
• Haukioja A. Probiotics and oral health. Eur J Dent. 2010;4(3):348–355.
   PubMedGoogle Scholar
• Saxelin M, Tynkkynen S, Mattila-Sandholm T, et al. Probiotic and other functional microbes: from markets to mechanisms. Curr Opin Biotechnol. 2005;16(2):204–211.
   PubMed Web of Science ®Google Scholar
• de Vrese M, Schrezenmeir J. Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol. 2008;111:1–66. doi:10.1007/10_2008_097
   Google Scholar
• Näse L, Hatakka K, Savilahti E, et al. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children. Caries Res. 2001;35(6):412–420.
   PubMed Web of Science ®Google Scholar
• Ahola A, Yli-Knuuttila H, Suomalainen T, et al. Short-term consumption of probiotic-containing cheese and its effect on dental caries risk factors. Arch Oral Biol. 2002;47(11):799–804.
   PubMed Web of Science ®Google Scholar
• Caglar E, Kavaloglu Cildir S, Ergeneli S, et al. Salivary mutans streptococci and lactobacilli levels after ingestion of the probiotic bacterium Lactobacillus reuteri ATCC 55730 by straws or tablets. Acta Odontol Scand. 2006;64(5):314–318.
   PubMed Web of Science ®Google Scholar
• Caglar E, Kavaloglu S, Kuscu O, et al. Effect of chewing gums containing xylitol or probiotic bacteria on salivary mutans streptococci and lactobacilli. Clin Oral Invest. 2007;11(4):425–429.
   PubMed Web of Science ®Google Scholar
• Twetman S, Derawi B, Keller M, et al. Short-term effect of chewing gums containing probiotic Lactobacillus reuteri on the levels of inflammatory mediators in gingival crevicular fluid. Acta Odontol Scand. 2009;67(1):19–24.
   PubMed Web of Science ®Google Scholar
• Tsubura S, Mizunuma H, Ishikawa S, et al. The effect of Bacillus subtilis mouth rinsing in patients with periodontitis. Eur J Clin Microbiol Infect Dis. 2009;28(11):1353–1356.
   PubMed Web of Science ®Google Scholar
• Burne R. Oral streptococci. products of their environment. J Dent Res. 1998;77(3):445–452.
   PubMed Web of Science ®Google Scholar
• Ajdic D, McShan WM, McLaughlin RE, et al. Genome sequence of Streptococcus mutans UA159, a cariogenic dental pathogen [Research Support, U.S. Gov't, P.H.S.]. Proc Natl Acad Sci Usa. 2002;99(22):14434–14439.
   PubMed Web of Science ®Google Scholar
• Lemos JA, Quivey RG, Jr Koo H, et al. Streptococcus mutans: a new Gram-positive paradigm? Microbiology (Reading)). 2013;159(Pt 3):436–445.
   PubMed Web of Science ®Google Scholar
• Muñoz-Sandoval C, Muñoz-Cifuentes MJ, Giacaman RA, et al. Effect of bovine milk on Streptococcus mutans biofilm cariogenic properties and enamel and dentin demineralization. Pediatric Dentistry. 2012;34(7):197E–201E.
   Google Scholar
• Liu C, Niu Y, Zhou X, et al. Hyperosmotic response of streptococcus mutans: from microscopic physiology to transcriptomic profile. BMC Microbiol. 2013;13(1):275
   PubMedGoogle Scholar
• Giacaman R. Sugars and beyond. The role of sugars and the other nutrients and their potential impact on caries. Oral Dis. 2018;24(7):1185–1197.
   PubMed Web of Science ®Google Scholar
• Boyd DA, Thevenot T, Gumbmann M, et al. Identification of the operon for the sorbitol (glucitol) phosphoenolpyruvate: sugar phosphotransferase system in Streptococcus mutans. Infect Immun. 2000;68(2):925–930.
   PubMed Web of Science ®Google Scholar
• Mäkinen KK. Sugar alcohol sweeteners as alternatives to sugar with special consideration of xylitol. Med Princ Pract. 2011;20(4):303–320.
   PubMed Web of Science ®Google Scholar
• Shemesh M, Tam A, Feldman M, et 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.
   PubMed Web of Science ®Google Scholar
• Yasbin RE, Young FE. Transduction in Bacillus subtilis by bacteriophage SPP1. J Virol. 1974;14(6):1343–1348.
   PubMed Web of Science ®Google Scholar
• Harwood C, Cutting S. Chemically defined growth media and supplements. Chichester, UK: Wiley; 1990.
   Google Scholar
• Assaf D, Steinberg D, Shemesh M. Lactose triggers biofilm formation by Streptococcus mutans. Int Dairy J. 2015;42:51–57.
   Web of Science ®Google Scholar
• Belli W, Marquis R. Catabolite modification of acid tolerance of Streptococcus mutans GS-5. Oral Microbiol Immunol. 1994;9(1):29–34.
   PubMedGoogle Scholar
• Duanis-Assaf D, Duanis-Assaf T, Zeng G, et al. Cell wall associated protein TasA provides an initial binding component to extracellular polysaccharides in dual-species biofilm. Sci Rep. 2018;8(1):9350
   PubMedGoogle Scholar
• Pratt LA, Kolter R. Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol. 1998;30(2):285–293.
   PubMed Web of Science ®Google Scholar
• Stepanović S, Vuković D, Dakić I, et al. A modified microtiter-plate test for quantification of staphylococcal biofilm formation. J Microbiol Methods. 2000;40(2):175–179.
   PubMed Web of Science ®Google Scholar
• Tam A, Shemesh M, Wormser U, et al. Effect of different iodine formulations on the expression and activity of Streptococcus mutans glucosyltransferase and fructosyltransferase in biofilm and planktonic environments. J Antimicrob Chemother. 2006;57(5):865–871.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Feldman M, Shenderovich J, Lavy E, et al. A sustained-release membrane of thiazolidinedione-8: effect on formation of a candida/bacteria mixed biofilm on hydroxyapatite in a continuous flow model. BioMed Res Int. 2017;2017:1–9.
   Web of Science ®Google Scholar
• Urbanczyk-Wochniak E, Leisse A, Roessner-Tunali U, et al. Expression of a bacterial xylose isomerase in potato tubers results in an altered hexose composition and a consequent induction of metabolism. Plant Cell Physiol. 2003;44(12):1359–1367.
   PubMed Web of Science ®Google Scholar
• Lisec J, Schauer N, Kopka J, et al. Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc. 2006;1(1):387–396.
   PubMed Web of Science ®Google Scholar
• Ng K, Ye R, Wu X-C, et al. Sorbitol dehydrogenase from Bacillus subtilis. Purification, characterization, and gene cloning. J Biol Chem. 1992;267(35):24989–24994.
   PubMed Web of Science ®Google Scholar
• Horwitz SB. D-Mannitol 1-phosphate dehydrogenase and d-sorbitol dehydrogenase from Bacillus subtilis. Methods Enzymol. 1966;9:155–159. Vol. Elsevier;
   Google Scholar
• Grela E, Kozłowska J, Grabowiecka A. Current methodology of MTT assay in bacteria–A review. Acta Histochem. 2018;120(4):303–311.
   PubMed Web of Science ®Google Scholar
• Cueva C, Moreno-Arribas MV, Martín-Álvarez PJ, et al. Antimicrobial activity of phenolic acids against commensal, probiotic and pathogenic bacteria. Res Microbiol. 2010;161(5):372–382.
   PubMed Web of Science ®Google Scholar
• Elias S, Banin E. Multi-species biofilms: living with friendly neighbors. FEMS Microbiol Rev. 2012;36(5):990–1004.
   PubMed Web of Science ®Google Scholar
• Burmølle M, Ren D, Bjarnsholt T, et al. Interactions in multispecies biofilms: do they actually matter? Trends Microbiol. 2014;22(2):84–91.
   PubMed Web of Science ®Google Scholar
• Fouet A, Arnaud M, Klier A, et al. Bacillus subtilis sucrose-specific enzyme II of the phosphotransferase system: expression in Escherichia coli and homology to enzymes II from enteric bacteria. Proc Natl Acad Sci Usa. 1987;84(24):8773–8777.
   PubMed Web of Science ®Google Scholar
• Fall R, Kinsinger RF, Wheeler KA. A simple method to isolate biofilm-forming Bacillus subtilis and related species from plant roots. Syst Appl Microbiol. 2004;27(3):372–379.
   PubMed Web of Science ®Google Scholar
• Vullo DL, Coto CE, Sineriz F. Characteristics of an inulinase produced by Bacillus subtilis 430A, a strain isolated from the rhizosphere of Vernonia herbacea (Vell Rusby). Appl Environ Microbiol. 1991;57(8):2392–2394.
   PubMed Web of Science ®Google Scholar
• Beauregard PB, Chai Y, Vlamakis H, et al. Bacillus subtilis biofilm induction by plant polysaccharides. Proc Natl Acad Sci Usa. 2013;110(17):E1621–E1630.
   PubMed Web of Science ®Google Scholar
• Parvaiz A, Satyawati S. Salt stress and phyto-biochemical responses of plants-a review. Plant Soil Environ. 2008;54(No. 3):89–99.
   Web of Science ®Google Scholar
• Dills SS, Seno S. Regulation of hexitol catabolism in Streptococcus mutans. J Bacteriol. 1983;153(2):861–866.
   PubMed Web of Science ®Google Scholar
• Brown A, Wittenberger C. Mannitol and sorbitol catabolism in Streptococcus mutans. Arch Oral Biol. 1973;18(1):117–IN19.
   PubMed Web of Science ®Google Scholar
• Slee A, Tanzer J. The repressible metabolism of sorbitol (D-glucitol) by intact cells of the oral plaque-forming bacterium Streptococcus mutans. Arch Oral Biol. 1983;28(9):839–845.
   PubMed Web of Science ®Google Scholar
• Svensäter G. Sorbitol transport and metabolism by oral streptococci. Swed Dent J Suppl. 1991;79:1–103.
   PubMedGoogle Scholar
• Durso SC, Vieira L, Cruz J, et al. Sucrose substitutes affect the cariogenic potential of Streptococcus mutans biofilms. Caries Res. 2014;48(3):214–222.
   PubMed Web of Science ®Google Scholar
• Lopez J, Thoms B. Role of sugar uptake and metabolic intermediates on catabolite repression in Bacillus subtilis. J Bacteriol. 1977;129(1):217–224.
   PubMed Web of Science ®Google Scholar
• Watanabe S, Hamano M, Kakeshita H, et al. Mannitol-1-phosphate dehydrogenase (MtlD) is required for mannitol and glucitol assimilation in Bacillus subtilis: possible cooperation of mtl and gut operons. J Bacteriol. 2003;185(16):4816–4824.
   PubMed Web of Science ®Google Scholar
• Heravi KM, Wenzel M, Altenbuchner J. Regulation of mtl operon promoter of Bacillus subtilis: requirements of its use in expression vectors. Microb Cell Fact. 2011;10(1):83.
   PubMedGoogle Scholar