Mechanical properties of a mature biofilm from a wastewater system: from microscale to macroscale level

References

• Abe Y, Polyakov P, Skali-Lami S, Francius G. 2011. Elasticity and physico-chemical properties during drinking water biofilm formation. Biofouling. 27:739–750.10.1080/08927014.2011.601300
   PubMed Web of Science ®Google Scholar
• Aggarwal S, Hozalski RM. 2012. Effect of strain rate on the mechanical properties of Staphylococcus epidermidis biofilms. Langmuir. 28:2812–2816.10.1021/la204342q
   PubMed Web of Science ®Google Scholar
• Ahimou F, Semmens MJ, Novak PJ, Haugstad G. 2007. Biofilm cohesiveness measurement using a novel atomic force microscopy methodology. Appl Environ Microbiol. 73:2897–2904.10.1128/AEM.02388-06
   PubMed Web of Science ®Google Scholar
• Allison DG, McBain AJ, Gilbert P. 2000. Biofilms: problems of control. In: Allison DG, Gilbert P, Lappin-Scott HM, Wilson M, editors. Symposia-society for general microbiology. Cambridge: Cambridge University Press; p. 309–328.
   Google Scholar
• Böl M, Ehret AE, Bolea Albero A, Hellriegel J, Krull R. 2013. Recent advances in mechanical characterisation of biofilm and their significance for material modelling. Crit Rev Biotechnol. 33:145–171.10.3109/07388551.2012.679250
   PubMed Web of Science ®Google Scholar
• Briscoe B, Fiori L, Pelillo E. 1998. Nano-indentation of polymeric surfaces. J Phys D: Appl Phys. 31:2395–2405.10.1088/0022-3727/31/19/006
   Web of Science ®Google Scholar
• Bryers JD. 2008. Medical biofilms. Biotechnol Bioeng. 100:1–18.10.1002/(ISSN)1097-0290
   PubMed Web of Science ®Google Scholar
• Cense A, Peeters E, Gottenbos B, Baaijens F, Nuijs A, van Dongen M. 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, Marshall KC. 1990. Biofilms. In: Characklis WG, Marshall KC, editors. Biofilms: a basis for an interdisciplinary approach. New York (NY): Wiley InterScience; p. 3–15.
   Google Scholar
• Clark AH, Ross-Murphy SB. 1985. The concentration dependence of biopolymer gel modulus. Br Polym J. 17:164–168.10.1002/(ISSN)1934-256X
   Web of Science ®Google Scholar
• Costerton JW, Cheng K, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ. 1987. Bacterial biofilms in nature and disease. Annu Rev Microbiol. 41:435–464.10.1146/annurev.mi.41.100187.002251
   PubMed Web of Science ®Google Scholar
• Demirdžić I, Džaferović E, Ivanković A. 2005. Finite-volume approach to thermoviscoelasticity. Numer Heat Transfer B-Fundam. 47:213–237.
   Web of Science ®Google Scholar
• Derlon N, Massé A, Escudié R, Bernet N, Paul E. 2008. Stratification in the cohesion of biofilms grown under various environmental conditions. Water Res. 42:2102–2110.10.1016/j.watres.2007.11.016
   PubMed Web of Science ®Google Scholar
• Dooling PJ, Buckley CP, Hinduja S. 1997. An intermediate model method for obtaining a discrete relaxation spectrum from creep data. Rheol Acta. 36:472–482.10.1007/BF00396332
   Web of Science ®Google Scholar
• Dunsmore B, Jacobsen A, Hall-Stoodley L, Bass C, Lappin-Scott H, Stoodley P. 2002. The influence of fluid shear on the structure and material properties of sulphate-reducing bacterial biofilms. J Ind Micribiol Biotechnol. 29:347–353.10.1038/sj.jim.7000302
   PubMed Web of Science ®Google Scholar
• Flemming H-C, Wingender J. 2010. The biofilm matrix. Nat Rev Microbiol. 8:623–633.
   PubMed Web of Science ®Google Scholar
• Geddes A. 2000. Infection in the twenty-first century: predictions and postulates. J Antimicrob Chemother. 46:873–877.10.1093/jac/46.6.873
   PubMed Web of Science ®Google Scholar
• Gilhawley F. 2008. Factors governing nitrification in an activated sludge system treating a pharmaceutical wastewater [thesis]. Dublin: School of Biotechnology, Dublin City University.
   Google Scholar
• Greaves GN, Greer AL, Lakes RS, Rouxel T. 2011. Poisson's ratio and modern materials. Nat Mater. 10:23–837.
   Google Scholar
• Grunlan JC, Xia X, Rowenhorst D, Gerberich WW. 2001. Preparation and evaluation of tungsten tips relative to diamond for nanoindentation of soft materials. Rev Sci Instrum. 72:2804–2810.10.1063/1.1370564
   Web of Science ®Google Scholar
• Gupta S, Carrillo F, Li C, Pruitt L, Puttlitz C. 2007. Adhesive forces significantly affect elastic modulus determination of soft polymeric materials in nanoindentation. Mater Lett. 61:448–451.10.1016/j.matlet.2006.04.078
   Web of Science ®Google Scholar
• He Y, Peterson BW, Jongsma MA, Ren Y, Sharma PK, Busscher HJ, Van der Mei HC. 2013. Stress relaxation analysis facilitates a quantitative approach towards antimicrobial penetration into biofilms. PLoS One. 8:e63750.10.1371/journal.pone.0063750
   PubMed Web of Science ®Google Scholar
• Hertz H. 1896. Über die Berührung Fester Elastischer Körper [On the contact of elastic solids]. J Reine Angew Mathematik. 92:39–60.
   Google Scholar
• Horn H, Reiff H, Morgenroth E. 2003. Simulation of growth and detachment in biofilm systems under defined hydrodynamic conditions. Biotechnol Bioeng. 81:607–617.10.1002/(ISSN)1097-0290
   PubMed Web of Science ®Google Scholar
• Hutter JL, Bechhoefer J. 1993. Calibration of atomic force microscope tips. Rev Sci Instrum. 64:1868–1873.10.1063/1.1143970
   Web of Science ®Google Scholar
• Jiang W, Wei Y, Gao X, Gao C, Wang Y. 2015. An innovative backwash cleaning technique for NF membrane in groundwater desalination: fouling reversibility and cleaning without chemical detergent. Desalination. 359:26–36.10.1016/j.desal.2014.12.025
   Web of Science ®Google Scholar
• Jiao Y, Cody GD, Harding AK, Wilmes P, Schrenk M, Wheeler KE, Banfield JF, Thelen MP. 2010. Characterization of extracellular polymeric substances from acidophilic microbial biofilms. Appl Environ Microbiol. 76:2916–2922.10.1128/AEM.02289-09
   PubMed Web of Science ®Google Scholar
• Jones RM. 1998. Mechanics of composite materials. Philadelphia (PA): CRC Press.
   Google Scholar
• Körstgens V, Flemming H, Wingender J, Borchard W. 2001. Influence of calcium ions on the mechanical properties of a model biofilm of mucoid Pseudomonas aeruginosa. Water Sci Technol. 43:49–57.
   PubMed Web of Science ®Google Scholar
• Lakes RS. 1998. Viscoelastic solids. Boca Raton (FL): CRC Press.
   Google Scholar
• Laspidou C, Aravas N. 2007. Variation in the mechanical properties of a porous multi-phase biofilm under compression due to void closure. Water Sci Technol. 55:447–453.10.2166/wst.2007.289
   PubMed Web of Science ®Google Scholar
• Lau PC, Dutcher JR, Beveridge TJ, Lam JS. 2009. Absolute quantitation of bacterial biofilm adhesion and viscoelasticity by microbead force spectroscopy. Biophys J. 96:2935–2948.10.1016/j.bpj.2008.12.3943
   PubMed Web of Science ®Google Scholar
• Mayer C, Moritz R, Kirschner C, Borchard W, Maibaum R, Wingender J, Flemming H-C. 1999. The role of intermolecular interactions: studies on model systems for bacterial biofilms. Int J Biol Macromol. 26:3–16.10.1016/S0141-8130(99)00057-4
   PubMed Web of Science ®Google Scholar
• Mosier AP, Kaloyeros AE, Cady NC. 2012. A novel microfluidic device for the in situ optical and mechanical analysis of bacterial biofilms. J Microbiol Methods. 91:198–204.10.1016/j.mimet.2012.07.006
   PubMed Web of Science ®Google Scholar
• Nguyen T, Roddick FA, Fan L. 2012. Biofouling of water treatment membranes: a review of the underlying causes, monitoring techniques and control measures. Membranes. 2:804–840.10.3390/membranes2040804
   PubMedGoogle Scholar
• Oh Y, Jo W, Yang Y, Park S. 2007. Influence of culture conditions on Escherichia coli O157: H7 biofilm formation by atomic force microscopy. Ultramicroscopy. 107:869–874.10.1016/j.ultramic.2007.01.021
   PubMed Web of Science ®Google Scholar
• Oh Y, Lee N, Jo W, Jung W, Lim J. 2009. Effects of substrates on biofilm formation observed by atomic force microscopy. Ultramicroscopy. 109:874–880.10.1016/j.ultramic.2009.03.042
   PubMed Web of Science ®Google Scholar
• Paramonova E, Kalmykowa OJ, Van der Mei HC, Busscher HJ, Sharma PK. 2009. Impact of hydrodynamics on oral biofilm strength. J Dent Res. 88:922–926.10.1177/0022034509344569
   PubMed Web of Science ®Google Scholar
• Peterson BW, Busscher HJ, Sharma PK, Van der Mei HC. 2012. Environmental and centrifugal factors influencing the visco-elastic properties of oral biofilms in vitro. Biofouling. 28:913–920.10.1080/08927014.2012.721515
   PubMedGoogle Scholar
• Peterson BW, Busscher HJ, Sharma PK, Van Der Mei HC. 2014. Visualization of microbiological process underlying stress relaxation in Pseudomonas aeruginosa biofilms. Microsc Microanal. 20:912–915.10.1017/S1431927614000361
   PubMed Web of Science ®Google Scholar
• Peterson BW, He Y, Ren Y, Zerdoum A, Libera M, Sharma PK, Van Winkelhoff A-J, Neut D, Stoodley P, Van der Mei HC, Busscher HJ. 2015. Viscoelasticity of biofilms and their recalcitrance to mechanical and chemical challenges. FEMS Microbiol Rev. 39:234–245.10.1093/femsre/fuu008
   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:e00497–00413.
   Google Scholar
• Reddy A, Trivedi J, Devmurari C, Mohan D, Singh P, Rao A, Joshi S, Ghosh P. 2005. Fouling resistant membranes in desalination and water recovery. Desalination. 183:301–306.10.1016/j.desal.2005.04.027
   Web of Science ®Google Scholar
• Rupp CJ, Fux CA, Stoodley P. 2005. Viscoelasticity of Staphylococcus aureus biofilms in response to fluid shear allows resistance to detachment and facilitates rolling migration. Appl Environ Microb. 71:2175–2178.10.1128/AEM.71.4.2175-2178.2005
   PubMed Web of Science ®Google Scholar
• Safari A. 2015. A combined experimental and numerical study of biofilm detachment. Dublin: University College Dublin.
   Google Scholar
• Safari A, Habimana O, Allen A, Casey E. 2014. The significance of calcium ions on Pseudomonas fluorescens biofilms – a structural and mechanical study. Biofouling. 30:859–869.10.1080/08927014.2014.938648
   PubMed Web of Science ®Google Scholar
• Schneider CA, Rasband WS, Eliceiri KW. 2012. NIH Image to ImageJ: 25 years of image analysis. Nat Methods. 9:671–675.10.1038/nmeth.2089
   PubMed Web of Science ®Google Scholar
• Stammen JA, Williams S, Ku DN, Guldberg RE. 2001. Mechanical properties of a novel PVA hydrogel in shear and unconfined compression. Biomaterials. 22:799–806.10.1016/S0142-9612(00)00242-8
   PubMed Web of Science ®Google Scholar
• Stewart PS, Franklin MJ. 2008. Physiological heterogeneity in biofilms. Nat Rev Microbiol. 6:199–210.10.1038/nrmicro1838
   PubMed Web of Science ®Google Scholar
• Stoodley P, Cargo R, Rupp CJ, Wilson S, Klapper I. 2002. Biofilm material properties as related to shear-induced deformation and detachment phenomena. J Ind Microbiol Biotechnol. 29:361–367.10.1038/sj.jim.7000282
   PubMed Web of Science ®Google Scholar
• Stoodley P, Lewandowski Z. 1994. Liquid flow in biofilm systems. Appl Environ Microbiol. 60:2711–2716.
   PubMed Web of Science ®Google Scholar
• Stoodley P, Lewandowski Z, Boyle JD, Lappin-Scott HM. 1999. Structural deformation of bacterial biofilms caused by short-term fluctuations in fluid shear: an in situ investigation of biofilm rheology. Biotechnol Bioeng. 65:83–92.10.1002/(ISSN)1097-0290
   PubMed Web of Science ®Google Scholar
• Stoodley P, Sauer K, Davies D, Costerton JW. 2002. Biofilms as complex differentiated communities. Annu Rev Microbiol. 56:187–209.10.1146/annurev.micro.56.012302.160705
   PubMed Web of Science ®Google Scholar
• Taherzadeh D, Picioreanu C, Küttler U, Simone A, Wall WA, Horn H. 2010. Computational study of the drag and oscillatory movement of biofilm streamers in fast flows. Biotechnol Bioeng. 105:600–610.10.1002/bit.v105:3
   PubMed Web of Science ®Google Scholar
• Telgmann U, Horn H, Morgenroth E. 2004. Influence of growth history on sloughing and erosion from biofilms. Water Res. 38:3671–3684.10.1016/j.watres.2004.05.020
   PubMed Web of Science ®Google Scholar
• Touhami A, Nysten B, Dufrêne YF. 2003. Nanoscale mapping of the elasticity of microbial cells by atomic force microscopy. Langmuir. 19:4539–4543.10.1021/la034136x
   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
• Tsoligkas AN, Bowen J, Winn M, Goss RJ, Overton TW, Simmons MJ. 2012. Characterisation of spin coated engineered Escherichia coli biofilms using atomic force microscopy. Colloids Surf B. 89:152–160.10.1016/j.colsurfb.2011.09.007
   PubMed Web of Science ®Google Scholar
• Van Loosdrecht M, Heijnen J, Eberl H, Kreft J, Picioreanu C. 2002. Mathematical modelling of biofilm structures. Antonie van Leeuwenhoek. 81:245–256.10.1023/A:1020527020464
   PubMed Web of Science ®Google Scholar
• Velegol SB, Logan BE. 2002. Contributions of bacterial surface polymers, electrostatics, and cell elasticity to the shape of AFM force curves. Langmuir. 18:5256–5262.10.1021/la011818g
   Web of Science ®Google Scholar
• Vinogradov A, Winston M, Rupp C, Stoodley P. 2004. Rheology of biofilms formed from the dental plaque pathogen Streptococcus mutans. Biofilms. 1:49–56.10.1017/S1479050503001078
   Google Scholar
• Volle C, Ferguson M, Aidala K, Spain E, Nunez M. 2008. Spring constants and adhesive properties of native bacterial biofilm cells measured by atomic force microscopy. Colloids Surf B. 67:32–40.10.1016/j.colsurfb.2008.07.021
   PubMed Web of Science ®Google Scholar
• Volle CB, Ferguson MA, Aidala KE, Spain EM, Núnez ME. 2008. Quantitative changes in the elasticity and adhesive properties of Escherichia coli ZK1056 prey cells during predation by Bdellovibrio bacteriovorus 109J. Langmuir. 24:8102–8110.10.1021/la8009354
   PubMed Web of Science ®Google Scholar
• Wilking JN, Angelini TE, Seminara A, Brenner MP, Weitz DA. 2011. Biofilms as complex fluids. MRS Bull. 36:385–391.10.1557/mrs.2011.71
   Web of Science ®Google Scholar
• Williams DL, Bloebaum RD. 2010. Observing the biofilm matrix of Staphylococcus epidermidis ATCC 35984 grown using the CDC biofilm reactor. Microsc Microanal. 16:143–152.10.1017/S143192760999136X
   PubMed Web of Science ®Google Scholar
• Williams J, Gamonpilas C. 2008. Using the simple compression test to determine Young’s modulus, Poisson’s ratio and the Coulomb friction coefficient. Int J Solids Struct. 45:4448–4459.10.1016/j.ijsolstr.2008.03.023
   Web of Science ®Google Scholar
• Wingender J, Neu TR, Flemming H-C, editors. 1999. Microbial extracellular polymeric substances: characterization, structure, and function. Berlin: Springer.10.1007/978-3-642-60147-7
   Google Scholar
• Yanagi C, Mori K. 1980. Advanced reverse osmosis process with automatic sponge ball cleaning for the reclamation of municipal sewage. Desalination. 32:391–398.10.1016/S0011-9164(00)86039-7
   Web of Science ®Google Scholar