Analysis of the mechanical stability and surface detachment of mature Streptococcus mutans biofilms by applying a range of external shear forces

References

• Balakrishnan M, Simmonds RS, Tagg JR. 2000. Dental caries is a preventable infectious disease. Aust Dent J. 45:235–245.10.1111/j.1834-7819.2000.tb00257.x
   PubMed Web of Science ®Google Scholar
• Beech IB, Sunner J. 2004. Biocorrosion: towards understanding interactions between biofilms and metals. Curr Opin Biotechnol. 15:181–186.10.1016/j.copbio.2004.05.001
   PubMed Web of Science ®Google Scholar
• Bird RB, Stewart WE, Lightfoot EN. 2002. Transport phenomena. 2nd ed. New York (NY): Wiley.
   Google Scholar
• Bourne MC. 2002. Food texture and viscosity: concept and measurement. San Diego (CA): Academic Press; p. 14–31.
   Google Scholar
• Bowen WH, Koo H. 2011. Biology of Streptococcus mutans-derived glucosyltransferases: role in extracellular matrix formation of cariogenic biofilms. Caries Res. 45:69–86.10.1159/000324598
   PubMed Web of Science ®Google Scholar
• Branda SS, Vik Å, Friedman L, Kolter R. 2005. Biofilms: the matrix revisited. Trends Microbiol. 13:20–26.10.1016/j.tim.2004.11.006
   PubMed Web of Science ®Google Scholar
• Busscher HJ, Van der Mei HC. 2006. Microbial adhesion in flow displacement systems. Clin Microbiol Rev. 19:127–141.10.1128/CMR.19.1.127-141.2006
   PubMed Web of Science ®Google Scholar
• Cense AW, Peeters EAG, Gottenbos B, Baaijens FPT, Nuijs AM, van Dongen MEH. 2006. Mechanical properties and failure of Streptococcus mutans biofilms, studied using a microindentation device. J Microbiol Methods. 67:463–472.10.1016/j.mimet.2006.04.023
   PubMed Web of Science ®Google Scholar
• Characklis WG, Turakhia MH, Zelver N. 1990. Transport and interfacial transfer phenomena. In: Characklis WG, Marshall KC, editors. Biofilms. New York (NY): John Wiley & Sons; p. 288–289.
   Google Scholar
• Cross SE, Kreth J, Zhu L, Sullivan R, Shi W, Qi F, Gimzewski JK. 2007. Nanomechanical properties of glucans and associated cell-surface adhesion of streptococcus mutans probed by atomic force microscopy under in situ conditions. Microbiology. 153:3124–3132.10.1099/mic.0.2007/007625-0
   PubMed Web of Science ®Google Scholar
• Darby R. 2001. Chemical engineering fluid mechanics. 2nd ed., revised and expanded ed. New York (NY): Marcel Dekker.
   Google Scholar
• Das T, Sharma PK, Krom BP, van der Mei HC, Busscher HJ. 2011. Role of eDNA on the adhesion forces between streptococcus mutans and substratum surfaces: influence of ionic strength and substratum hydrophobicity. Langmuir. 27:10113–10118.10.1021/la202013m
   PubMed Web of Science ®Google Scholar
• Demirci M, Tuncer S, Yuceokur AA. 2010. Prevalence of caries on individual tooth surfaces and its distribution by age and gender in university clinic patients. Eur J Dent. 4:270–279.
   PubMedGoogle Scholar
• Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G, Eke PI, Beltrán-Aguilar ED, Horowitz AM, Li C-H. 2007. Trends in oral health status: United States, 1988–1994 and 1999–2004. National Center for Health Statistics. Vital Health Stat. 11:1–92.
   Google Scholar
• Flemming H, Wingender J. 2010. The biofilm matrix. Nat Rev. Micro. 8:623–633.
   Google Scholar
• Galy O, Latour-Lambert P, Zrelli K, Ghigo J, Beloin C, Henry N. 2012. Mapping of bacterial biofilm local mechanics by magnetic microparticle actuation. Biophys J. 103:1400–1408.10.1016/j.bpj.2012.07.001
   PubMed Web of Science ®Google Scholar
• Gottenbos B, Van der Mei HC, Busscher HJ. 1999. Models for studying initial adhesion and surface growth in biofilm formation on surfaces. Meth Enzymol. 310:523–534.10.1016/S0076-6879(99)10040-5
   PubMed Web of Science ®Google Scholar
• Guggenheim B, Guggenheim M, Gmür R, Giertsen E, Thurnheer T. 2004. Application of the Zürich biofilm model to problems of cariology. Caries Res. 38:212–222.10.1159/000077757
   PubMed Web of Science ®Google Scholar
• Guo L, Hu W, He X, Lux R, McLean J, Shi W. 2013. Investigating acid production by Streptococcus mutans with a surface-displayed pH-sensitive green fluorescent protein. PLoS One. 8:e57182.10.1371/journal.pone.0057182
   PubMed Web of Science ®Google Scholar
• Hall-Stoodley L, Costerton JW, Stoodley P. 2004. Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Micro. 2:95–108.10.1038/nrmicro821
   PubMed Web of Science ®Google Scholar
• Hayacibara MF, Koo H, Vacca Smith AM, Kopec LK, Scott-Anne K, Cury JA, Bowen WH. 2004. The influence of mutanase and dextranase on the production and structure of glucans synthesized by streptococcal glucosyltransferases. Carbohydr Res. 339:2127–2137.10.1016/j.carres.2004.05.031
   PubMed Web of Science ®Google Scholar
• Hull PS. 1980. Chemical inhibition of plaque. J Clin Periodontol. 7:431–442.10.1111/cpe.1980.7.issue-6
   PubMed Web of Science ®Google Scholar
• Jiao BH, Li WJ, Fang YW, Liu S. 2014. Characterization of a marine-derived dextranase and its application to the prevention of dental caries. J Ind Microbiol Biotechnol. 41:17–26.10.1007/s10295-013-1369-0
   PubMed Web of Science ®Google Scholar
• Klapper I, Rupp CJ, Cargo R, Purvedorj B, Stoodley P. 2002. Viscoelastic fluid description of bacterial biofilm material properties. Biotechnol Bioeng. 80:289–296.10.1002/(ISSN)1097-0290
   PubMed Web of Science ®Google Scholar
• Klein MI, Duarte S, Xiao J, Mitra S, Foster TH, Koo H. 2009. Structural and molecular basis of the role of starch and sucrose in Streptococcus mutans biofilm development. Appl Environ Microbiol. 75:837–841.10.1128/AEM.01299-08
   PubMed Web of Science ®Google Scholar
• Klein MI, DeBaz L, Agidi S, Lee H, Xie G, Lin AHM, Hamaker BR, Lemos JA, Koo H. 2010. Dynamics of Streptococcus mutans transcriptome in response to starch and sucrose during Bbofilm development. PLoS One. 5:e13478.10.1371/journal.pone.0013478
   PubMed Web of Science ®Google Scholar
• Koo H, Falsetta ML, Klein MI. 2013. The exopolysaccharide matrix: a virulence determinant of cariogenic biofilm. J Dent Res. 92:1065–1073.10.1177/0022034513504218
   PubMed Web of Science ®Google Scholar
• Koo H, Hayacibara MF, Schobel BD, Cury JA, Rosalen PL, Park YK, Vacca-Smith AM, Bowen WH. 2003. Inhibition of Streptococcus mutans biofilm accumulation and polysaccharide production by apigenin and tt-farnesol. J Antimicrob Chemother. 52:782–789.10.1093/jac/dkg449
   PubMed Web of Science ®Google Scholar
• Koo H, Xiao J, Klein MI, Jeon JG. 2010. Exopolysaccharides produced by Streptococcus mutans glucosyltransferases modulate the establishment of microcolonies within multispecies biofilms. J Bacteriol. 192:3024–3032.10.1128/JB.01649-09
   PubMed Web of Science ®Google Scholar
• Kopec LK, Vacca-Smith AM, Bowen WH. 1997. Structural aspects of glucans formed in solution and on the surface of hydroxyapatite. Glycobiology. 7:929–934.10.1093/glycob/7.7.929
   PubMed Web of Science ®Google Scholar
• Körstgens V, Flemming H, Wingender J, Borchard W. 2001. Uniaxial compression measurement device for investigation of the mechanical stability of biofilms. J Microbiol Methods. 46:9–17.10.1016/S0167-7012(01)00248-2
   PubMed Web of Science ®Google Scholar
• Kostakioti M, Hadjifrangiskou M, Hultgren SJ. 2013. Bacterial biofilms: development, dispersal, and therapeutic strategies in the dawn of the postantibiotic era. Cold Spring Harb Perspect Med. 3:a010306.
   PubMed Web of Science ®Google Scholar
• Kreth J, Hagerman E, Tam K, Merritt J, Wong DTW, Wu BM, Myung NV, Shi W, Qi F. 2004. Quantitative analyses of Streptococcus mutans biofilms with quartz crystal microbalance, microjet impingement and confocal microscopy. Biofilms. 1:277–284.10.1017/S1479050504001516
   PubMedGoogle Scholar
• Kreth J, Zhu L, Merritt J, Shi W, Qi F. 2008. Role of sucrose in the fitness of Streptococcus mutans. Oral Microbiol Immunol. 23:213–219.10.1111/j.1399-302X.2007.00413.x
   PubMedGoogle Scholar
• Lau PCY, Lindhout T, Beveridge TJ, Dutcher JR, Lam JS. 2009. Differential lipopolysaccharide core capping leads to quantitative and correlated modifications of mechanical and structural properties in Pseudomonas aeruginosa biofilms. J Bacteriol. 191:6618–6631.10.1128/JB.00698-09
   PubMed Web of Science ®Google Scholar
• Lynch DJ, Fountain TL, Mazurkiewicz JE, Banas JA. 2007. Glucan-binding proteins are essential for shaping Streptococcus mutans biofilm architecture. FEMS Microbiol Lett. 268:158–165.10.1111/fml.2007.268.issue-2
   PubMed Web of Science ®Google Scholar
• Mann EE, Wozniak DJ. 2012. Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev. 36:893–916.10.1111/j.1574-6976.2011.00322.x
   PubMed Web of Science ®Google Scholar
• Marsh PD, Moter A, Devine DA. 2011. Dental plaque biofilms: communities, conflict and control. Periodontol 2000. 55:16–35.10.1111/prd.2010.55.issue-1
   PubMed Web of Science ®Google Scholar
• Martines E, McGhee K, Wilkinson C, Curtis A. 2004. A parallel-plate flow chamber to study initial cell adhesion on a nanofeatured surface. IEEE Trans Nanobioscience. 3:90–95.10.1109/TNB.2004.828268
   PubMed Web of Science ®Google Scholar
• McCabe WL, Smith JC. 1976. Unit operations of chemical engineering. New York (NY): McGraw-Hill.
   Google Scholar
• Mert B, Campanella OH. 2008. The study of the mechanical impedance of foods and biomaterials to characterize their linear viscoelastic behavior at high frequencies. Rheol Acta. 47:727–737.10.1007/s00397-008-0277-0
   Web of Science ®Google Scholar
• Monds RD, O’Toole GA. 2009. The developmental model of microbial biofilms: ten years of a paradigm up for review. Trends Microbiol. 17:73–87.10.1016/j.tim.2008.11.001
   PubMed Web of Science ®Google Scholar
• O’Toole G, Kaplan HB, Kolter R. 2000. Biofilm formation as microbial development. Annu Rev Microbiol. 54:49–79.10.1146/annurev.micro.54.1.49
   PubMed Web of Science ®Google Scholar
• Paes Leme AF, Koo H, Bellato CM, Bedi G, Cury JA. 2006. The role of sucrose in cariogenic dental biofilm formation – new insight. J Dent Res. 85:878–887.10.1177/154405910608501002
   PubMed Web of Science ®Google Scholar
• Peterson BW, van der Mei HC, Sjollema J, Busscher HJ, Sharma PK. 2013. A distinguishable role of eDNA in the viscoelastic relaxation of biofilms. mBio 4:e00497–13.
   PubMed Web of Science ®Google Scholar
• Rmaile A, Carugo D, Capretto L, Aspiras M, De Jager M, Ward M, Stoodley P. 2014. Removal of interproximal dental biofilms by high-velocity water microdrops. J Dent Res. 93:68–73.10.1177/0022034513510945
   PubMed Web of Science ®Google Scholar
• Shaw T, Winston M, Rupp CJ, Klapper I, Stoodley P. 2004. Commonality of elastic relaxation times in biofilms. Phys Rev Lett. 93:098102.10.1103/PhysRevLett.93.098102
   PubMed Web of Science ®Google Scholar
• Shumi W, Kim SH, Lim J, Cho K, Han H, Park S. 2013. Shear stress tolerance of Streptococcus mutans aggregates determined by microfluidic funnel device (μFFD). J Microbiol Methods. 93:85–89.10.1016/j.mimet.2013.02.004
   PubMed Web of Science ®Google Scholar
• Simões M, Simões LC, Cleto S, Pereira MO, Vieira MJ. 2008. The effects of a biocide and a surfactant on the detachment of Pseudomonas fluorescens from glass surfaces. Int J Food Microbiol. 121:335–341.10.1016/j.ijfoodmicro.2007.11.041
   PubMed Web of Science ®Google Scholar
• Stewart PS. 2014. Biophysics of biofilm infection. Pathog Dis. 70:212–218.
   Google Scholar
• Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Micro. 6:199–210.10.1038/nrmicro1838
   PubMed Web of Science ®Google Scholar
• Sumei L, Klein MI, Heim KP, Fan Y, Bitoun JP, Ahn SJ, Burne RA, Koo H, Brady LJ, Wen ZT. 2014. Streptococcus mutans eDNA is up-regulated during growth in biofilms, actively released via membrane vesicles, and influenced by components of the protein secretion machinery. J Bact. 196:2355–2366.
   PubMed Web of Science ®Google Scholar
• Towler BW, Rupp CJ, Cunningham AB, Stoodley P. 2003. Viscoelastic properties of a mixed culture biofilm from rheometer creep analysis. Biofouling. 19:279–285.10.1080/0892701031000152470
   PubMed Web of Science ®Google Scholar
• Vinogradov AM, Winston M, Rupp CJ, Stoodley P. 2004. Rheology of biofilms formed from the dental plaque pathogen Streptococcus mutans. Biofilms. 1:49–56.10.1017/S1479050503001078
   Google Scholar
• Waters MS, Kundu S, Lin NJ, Lin-Gibson S. 2014. Microstructure and mechanical properties of in situ Streptococcus mutans biofilms. ACS Appl Mater Interfaces. 6:327–332.10.1021/am404344h
   PubMed Web of Science ®Google Scholar
• Xiao J, Koo H. 2010. Structural organization and dynamics of exopolysaccharide matrix and microcolonies formation by Streptococcus mutans in biofilms. J Appl Microbiol. 108:2103–2113.
   PubMed Web of Science ®Google Scholar
• Xiao J, Klein MI, Falsetta ML, Lu B, Delahunty CM, Yates JRI, Heydorn A, Koo H. 2012. The exopolysaccharide matrix modulates the interaction between 3D architecture and virulence of a mixed-species oral biofilm. PLoS Pathog. 8:e1002623.10.1371/journal.ppat.1002623
   PubMed Web of Science ®Google Scholar