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Surface conditioning with Escherichia coli cell wall components can reduce biofilm formation by decreasing initial adhesion

  • Received: 14 April 2017 Accepted: 11 July 2017 Published: 18 July 2017
  • Bacterial adhesion and biofilm formation on food processing surfaces pose major risks to human health. Non-efficient cleaning of equipment surfaces and piping can act as a conditioning layer that affects the development of a new biofilm post-disinfection. We have previously shown that surface conditioning with cell extracts could reduce biofilm formation. In the present work, we hypothesized that E. coli cell wall components could be implicated in this phenomena and therefore mannose, myristic acid and palmitic acid were tested as conditioning agents. To evaluate the effect of surface conditioning and flow topology on biofilm formation, assays were performed in agitated 96-well microtiter plates and in a parallel plate flow chamber (PPFC), both operated at the same average wall shear stress (0.07 Pa) as determined by computational fluid dynamics (CFD). It was observed that when the 96-well microtiter plate and the PPFC were used to form biofilms at the same shear stress, similar results were obtained. This shows that the referred hydrodynamic feature may be a good scale-up parameter from high-throughput platforms to larger scale flow cell systems as the PPFC used in this study. Mannose did not have any effect on E. coli biofilm formation, but myristic and palmitic acid inhibited biofilm development by decreasing cell adhesion (in about 50%). These results support the idea that in food processing equipment where biofilm formation is not critical below a certain threshold, bacterial lysis and adsorption of cell components to the surface may reduce biofilm buildup and extend the operational time.

    Citation: Luciana C. Gomes, Joana M. R. Moreira, José D. P. Araújo, Filipe J. Mergulhão. Surface conditioning with Escherichia coli cell wall components can reduce biofilm formation by decreasing initial adhesion[J]. AIMS Microbiology, 2017, 3(3): 613-628. doi: 10.3934/microbiol.2017.3.613

    Related Papers:

  • Bacterial adhesion and biofilm formation on food processing surfaces pose major risks to human health. Non-efficient cleaning of equipment surfaces and piping can act as a conditioning layer that affects the development of a new biofilm post-disinfection. We have previously shown that surface conditioning with cell extracts could reduce biofilm formation. In the present work, we hypothesized that E. coli cell wall components could be implicated in this phenomena and therefore mannose, myristic acid and palmitic acid were tested as conditioning agents. To evaluate the effect of surface conditioning and flow topology on biofilm formation, assays were performed in agitated 96-well microtiter plates and in a parallel plate flow chamber (PPFC), both operated at the same average wall shear stress (0.07 Pa) as determined by computational fluid dynamics (CFD). It was observed that when the 96-well microtiter plate and the PPFC were used to form biofilms at the same shear stress, similar results were obtained. This shows that the referred hydrodynamic feature may be a good scale-up parameter from high-throughput platforms to larger scale flow cell systems as the PPFC used in this study. Mannose did not have any effect on E. coli biofilm formation, but myristic and palmitic acid inhibited biofilm development by decreasing cell adhesion (in about 50%). These results support the idea that in food processing equipment where biofilm formation is not critical below a certain threshold, bacterial lysis and adsorption of cell components to the surface may reduce biofilm buildup and extend the operational time.


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    [1] Giaouris ED, Heir E, Desvaux M, et al. (2015) Intra- and inter-species interactions within biofilms of important foodborne bacterial pathogens. Front Microbiol 6: 841.
    [2] Yaron S, Romling U (2014) Biofilm formation by enteric pathogens and its role in plant colonization and persistence. Microb Biotechnol 7: 496–516. doi: 10.1111/1751-7915.12186
    [3] Moreira JMR, Araújo JDP, Simões M, et al. (2016) Influence of surface conditioning with culture medium components on Escherichia coli biofilm formation, In: Henderson J, Editor, Biofilms: Characterization, Applications and Recent Advances, New York: Nova Science Publishers, Inc., 205–224.
    [4] Moreira JMR, Gomes LC, Whitehead KA, et al. (2017) Effect of surface conditioning with cellular extracts on Escherichia coli adhesion and initial biofilm formation. Food Bioprod Process 104: 1–12. doi: 10.1016/j.fbp.2017.03.008
    [5] Whitehead KA, Verran J (2015) Formation, architecture and functionality of microbial biofilms in the food industry. Curr Opin Food Sci 2: 84–91. doi: 10.1016/j.cofs.2015.02.003
    [6] Cloete TE (2003) Resistance mechanisms of bacteria to antimicrobial compounds. Int Biodeter Biodegr 51: 277–282. doi: 10.1016/S0964-8305(03)00042-8
    [7] Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT Food Sci Technol 43: 573–583. doi: 10.1016/j.lwt.2009.12.008
    [8] Coughlan LM, Cotter PD, Hill C, et al. (2016) New weapons to fight old enemies: novel strategies for the (bio)control of bacterial biofilms in the food industry. Front Microbiol 7: 1641.
    [9] Akbas MY (2015) Bacterial biofilms and their new control strategies in food industry, In: Méndez-Vilas A, Editor, The Battle Against Microbial Pathogens: Basic Science, Technological Advances and Educational Programs, Badajoz: Formatex, 383–394.
    [10] Bernbom N, Jørgensen RL, Ng YY, et al. (2006) Bacterial adhesion to stainless steel is reduced by aqueous fish extract coatings. Biofilms 3: 25–36.
    [11] Fletcher M (1976) The effects of proteins on bacterial attachment to polystyrene. J Gen Microbiol 94: 400–404. doi: 10.1099/00221287-94-2-400
    [12] Bower CK, McGuire J, Daeschel MA (1996) The adhesion and detachment of bacteria and spores on food-contact surfaces. Trends Food Sci Technol 7: 152–157. doi: 10.1016/0924-2244(96)81255-6
    [13] Wong ACL (1998) Biofilms in food processing environments. J Dairy Sci 81: 2765–2770. doi: 10.3168/jds.S0022-0302(98)75834-5
    [14] Robitaille G, Choinière S, Ells T, et al. (2014) Attachment of Listeria innocua to polystyrene: effects of ionic strength and conditioning films from culture media and milk proteins. J Food Prot 77: 427–434. doi: 10.4315/0362-028X.JFP-13-353
    [15] Dat NM, Manh LD, Hamanaka D, et al. (2014) Surface conditioning of stainless steel coupons with skim milk, buttermilk, and butter serum solutions and its effect on bacterial adherence. Food Control 42: 94–100. doi: 10.1016/j.foodcont.2014.01.040
    [16] Hamadi F, Asserne F, Elabed S, et al. (2014) Adhesion of Staphylococcus aureus on stainless steel treated with three types of milk. Food Control 38: 104–108. doi: 10.1016/j.foodcont.2013.10.006
    [17] Bernbom N, Ng YY, Jørgensen RL, et al. (2009) Adhesion of food-borne bacteria to stainless steel is reduced by food conditioning films. J Appl Microbiol 106: 1268–1279. doi: 10.1111/j.1365-2672.2008.04090.x
    [18] He X, Liu Y, Huang J, et al. (2015) Adsorption of alginate and albumin on aluminum coatings inhibits adhesion of Escherichia coli and enhances the anti-corrosion performances of the coatings. Appl Sci Res 332: 89–96.
    [19] Barnes LM, Lo MF, Adams MR, et al. (1999) Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl Environ Microbiol 65: 4543–4548.
    [20] Reynolds EC, Wong A (1983) Effect of adsorbed protein on hydroxyapatite zeta potential and Streptococcus mutans adherence. Infect Immun 39: 1285–1290.
    [21] Valle J, Da RS, Henry N, et al. (2006) Broad-spectrum biofilm inhibition by a secreted bacterial polysaccharide. Proc Natl Acad Sci USA 103: 12558–12563. doi: 10.1073/pnas.0605399103
    [22] Rendueles O, Travier L, Latour-Lambert P, et al. (2011) Screening of Escherichia coli species biodiversity reveals new biofilm-associated antiadhesion polysaccharides. mBio 2: e00043-11.
    [23] Donlan RM (2002) Biofilms: microbial life on surfaces. Emerg Infect Dis 8: 881–890. doi: 10.3201/eid0809.020063
    [24] Martinuzzi RJ, Salek MM (2010) Numerical simulation of fluid flow and hydrodynamic analysis in commonly used biomedical devices in biofilm studies, In: Angermann L, Editor, Numerical Simulations-Examples and Applications in Computational Fluid Dynamics, Rijeka: InTech, 193–212.
    [25] Busscher HJ, van der Mei HC (2006) Microbial adhesion in flow displacement systems. Clin Microbiol Rev 19: 127–141. doi: 10.1128/CMR.19.1.127-141.2006
    [26] Moreira JMR, Gomes LC, Araújo JDP, et al. (2013) The effect of glucose concentration and shaking conditions on Escherichia coli biofilm formation in microtiter plates. Chem Eng Sci 94: 192–199. doi: 10.1016/j.ces.2013.02.045
    [27] Gomes LC, Moreira JM, Teodósio JS, et al. (2014) 96-well microtiter plates for biofouling simulation in biomedical settings. Biofouling 30: 535–546. doi: 10.1080/08927014.2014.890713
    [28] Hu X, Shi Y, Zhang P, et al. (2016) D-Mannose: properties, production, and applications: an overview. Compr Rev Food Sci F 15: 773–785. doi: 10.1111/1541-4337.12211
    [29] Mangia AHR, Bergter EB, Teixeira LM, et al. (1999) A preliminary investigation on the chemical composition of the cell surface of five enteropathogenic Escherichia coli serotypes. Mem Inst Oswaldo Cruz 94: 513–518. doi: 10.1590/S0074-02761999000400016
    [30] Oursel D, Loutelier-Bourhis C, Orange N, et al. (2007) Identification and relative quantification of fatty acids in Escherichia coli membranes by gas chromatography/mass spectrometry. Rapid Commun Mass Spectrom 21: 3229–3233. doi: 10.1002/rcm.3177
    [31] Shokri A, Larsson G (2004) Characterisation of the Escherichia coli membrane structure and function during fedbatch cultivation. Microb Cell Fact 3: 9. doi: 10.1186/1475-2859-3-9
    [32] Gomes LC, Moreira JMR, Teodósio JS, et al. (2014) 96-well microtiter plates for biofouling simulation in biomedical settings. Biofouling 30: 1–12. doi: 10.1080/08927014.2013.836507
    [33] Teodósio JS, Simões M, Melo LF, et al. (2011) Flow cell hydrodynamics and their effects on E. coli biofilm formation under different nutrient conditions and turbulent flow. Biofouling 27: 1–11.
    [34] Moreira JMR, Ponmozhi J, Campos JBLM, et al. (2015) Micro and macro flow systems to study Escherichia coli adhesion to biomedical materials. Chem Eng Sci 126: 440–445. doi: 10.1016/j.ces.2014.12.054
    [35] Martinez LR, Casadevall A (2007) Cryptococcus neoformans biofilm formation depends on surface support and carbon source and reduces fungal cell susceptibility to heat, cold, and UV light. Appl Environ Microbiol 73: 4592–4601. doi: 10.1128/AEM.02506-06
    [36] Pratt-Terpstra IH, Weerkamp AH, Busscher HJ (1987) Adhesion of oral Streptococci from a flowing suspension to uncoated and albumin-coated surfaces. J Gen Microbiol 133: 3199–3206.
    [37] Moreira JMR, Araújo JDP, Miranda JM, et al. (2014) The effects of surface properties on Escherichia coli adhesion are modulated by shear stress. Colloids Surface B 123: 1–7. doi: 10.1016/j.colsurfb.2014.08.016
    [38] Moreira JMR, Gomes LC, Simões M, et al. (2015) The impact of material properties, nutrient load and shear stress on biofouling in food industries. Food Bioprod Process 95: 228–236. doi: 10.1016/j.fbp.2015.05.011
    [39] van OC (1994) Interfacial Forces in Aqueous Media, New York: Marcel Dekker Inc.
    [40] Janczuk B, Chibowski E, Bruque JM, et al. (1993) On the consistency of surface free energy components as calculated from contact angles of different liquids: an application to the cholesterol surface. ‎J Colloid Interf Sci 159: 421–428. doi: 10.1006/jcis.1993.1342
    [41] Salek M, Sattari P, Martinuzzi R (2012) Analysis of fluid flow and wall shear stress patterns inside partially filled agitated culture well plates. Ann Biomed Eng 40: 707–728. doi: 10.1007/s10439-011-0444-9
    [42] Pitts B, Hamilton MA, Zelver N, et al. (2003) A microtiter-plate screening method for biofilm disinfection and removal. J Microbiol Meth 54: 269–276. doi: 10.1016/S0167-7012(03)00034-4
    [43] Shakeri S, Kermanshahi RK, Moghaddam MM, et al. (2007) Assessment of biofilm cell removal and killing and biocide efficacy using the microtiter plate test. Biofouling 23: 79–86. doi: 10.1080/08927010701190011
    [44] Bridier A, Dubois-Brissonnet F, Boubetra A, et al. (2010) The biofilm architecture of sixty opportunistic pathogens deciphered using a high throughput CLSM method. J Microbiol Meth 82: 64–70. doi: 10.1016/j.mimet.2010.04.006
    [45] Trautner BW, Lopez AI, Kumar A, et al. (2012) Nanoscale surface modification favors benign biofilm formation and impedes adherence by pathogens. Nanomedicine 8: 261–270. doi: 10.1016/j.nano.2011.11.014
    [46] Rodrigues DF, Elimelech M (2009) Role of type 1 fimbriae and mannose in the development of Escherichia coli K12 biofilm: from initial cell adhesion to biofilm formation. Biofouling 25: 401–411. doi: 10.1080/08927010902833443
    [47] Pratt LA, Kolter R (1998) Genetic analysis of Escherichia coli biofilm formation: roles of flagella, motility, chemotaxis and type I pili. Mol Microbiol 30: 285–293. doi: 10.1046/j.1365-2958.1998.01061.x
    [48] Old DC (1972) Inhibition of the interaction between fimbrial haemagglutinins and erythrocytes by D-mannose and other carbohydrates. J Gen Microbiol 71: 149–157. doi: 10.1099/00221287-71-1-149
    [49] Duguid JP, Gillies RR (1957) Fimbrae and adhesive properties in dysentery bacilli. J Pathol 74: 397–411. doi: 10.1002/path.1700740218
    [50] Ofek I, Mirelman D, Sharon N (1977) Adherence of Escherichia coli to human mucosal cells mediated by mannose receptors. Nature 265: 623–625. doi: 10.1038/265623a0
    [51] Ofek I, Beachey EH, Sharon N (1978) Surface sugars of animal cells as determinants of recognition in bacterial adherence. Trends Biochem Sci 3: 159–160.
    52. Sharon N, Eshdat Y, Silverblatt FJ, et al. (1981) Bacterial adherence to cell surface sugars. Ciba Found Symp 80: 119–141. doi: 10.1016/S0968-0004(78)90294-3
    [52] 53. Pearce WA, Buchanan TM (1980) Structure and cell membrane-binding properties of bacterial fimbriae, In: Beachey EH, Editor, Bacterial Adherence, Dordrecht: Springer Netherlands, 289–344.
    [53] 54. Sharon N (1987) Bacterial lectins, cell-cell recognition and infectious disease. FEBS Lett 217: 145–157. doi: 10.1016/0014-5793(87)80654-3
    [54] 55. Whitehead KA, Smith LA, Verran J (2010) The detection and influence of food soils on microorganisms on stainless steel using scanning electron microscopy and epifluorescence microscopy. Int J Food Microbiol 141: S125–S133. doi: 10.1016/j.ijfoodmicro.2010.01.012
    [55] 56. Whitehead KA, Benson P, Smith LA, et al. (2009) The use of physicochemical methods to detect organic food soils on stainless steel surfaces. Biofouling 25: 749–756. doi: 10.1080/08927010903161299
    [56] 57. Inoue T, Shingaki R, Fukui K (2008) Inhibition of swarming motility of Pseudomonas aeruginosa by branched-chain fatty acids. FEMS Microbiol Lett 281: 81–86. doi: 10.1111/j.1574-6968.2008.01089.x
    [57] 58. Soni KA, Jesudhasan P, Cepeda M, et al. (2008) Identification of ground beef-derived fatty acid inhibitors of autoinducer-2-based cell signaling. J Food Prot 71: 134–138. doi: 10.4315/0362-028X-71.1.134
    [58] 59. Huang CB, George B, Ebersole JL (2010) Antimicrobial activity of n-6, n-7 and n-9 fatty acids and their esters for oral microorganisms. Arch Oral Biol 55: 555–560. doi: 10.1016/j.archoralbio.2010.05.009
    [59] 60. Wenderska IB, Chong M, McNulty J, et al. (2011) Palmitoyl-DL-carnitine is a multitarget inhibitor of Pseudomonas aeruginosa biofilm development. Chem Bio Chem 12: 272766. doi: 10.1002/cbic.201100500
    [60] 61. Dusane DH, Pawar VS, Nancharaiah YV, et al. (2011) Anti-biofilm potential of a glycolipid surfactant produced by a tropical marine strain of Serratia marcescens. Biofouling 27: 645–654. doi: 10.1080/08927014.2011.594883
    [61] 62. Liaw SJ, Lai HC, Wang WB (2004) Modulation of swarming and virulence by fatty acids through the RsbA protein in Proteus mirabilis. Infect Immun 72: 6836–6845. doi: 10.1128/IAI.72.12.6836-6845.2004
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