, Volume 23, Issue 2, pp 219–227 | Cite as

Physico-chemical approach to adhesion of Alicyclobacillus cells and spores to model solid materials

  • Jan Strejc
  • Lucie Kyselova
  • Anna Cadkova
  • Tomas Potocar
  • Tomas BranyikEmail author
Original Paper


Acidothermophilic bacteria of the genus Alicyclobacillus are frequent contaminants of fruit-based products. This study is the first attempt to characterize the physico-chemical surface properties of two Alicyclobacillus sp. and quantify their adhesion disposition to model materials [diethylaminoethyl (DEAE), carboxyl- and octyl-modified magnetic beads] representing materials with different surface properties used in the food industry. An insight into the mechanism of adhesion was gained through comparison of experimental adhesion intensities with predictions of a colloidal interaction model (XDLVO). Experimental data (contact angles, zeta potentials, size) on interacting surfaces (cells and materials) were used as inputs into the XDLVO model. The results revealed that the most significant adhesion occurred at pH 3. Adhesion of both vegetative cells and spores of two Alicyclobacillus sp. to all materials studied was the most pronounced under acidic conditions, and adhesion was influenced mostly by electrostatic attractions. The most intensive adhesion of vegetative cells and spores at pH 3 was observed for DEAE followed by hydrophobic octyl and hydrophilic carboxyl surfaces. Overall, the lowest rate of adhesion between cells and model materials was observed at an alkaline pH. Consequently, prevention of adhesion should be based on the use of alkaline sanitizers and/or alkaline rinse water.


Alicyclobacillus sp. Cell adhesion Model materials Surface interaction XDLVO model 



This research was supported by the Grant Agency of the Czech Republic through project 18-05007S.


  1. Abee T, Kovacs AT, Kuipers OP, Veen S (2011) Biofilm formation and dispersal in gram-positive bacteria. Curr Opin Biotech 22:172–179Google Scholar
  2. Azeredo DRP, Alvarenga V, Sant’Ana AS, Sabaa Srur AUO (2016) An overview of microorganisms and factors contributing for the microbial stability of carbonated soft drinks. Food Res Int 82:136–144Google Scholar
  3. Bevilacqua A, Sinigaglia M, Corbo MR (2008) Alicyclobacillus acidoterrestris: new methods for inhibiting spore germination. Int J Food Microbiol 125:103–110Google Scholar
  4. Bittner M, de Souza AC, Brozova M, Matoulkova D, Dias DR, Branyik T (2016) Adhesion of anaerobic beer spoilage bacteria Megasphaera cerevisiae and Pectinatus frisingensis to stainless steel. LWT Food Sci Technol 70:148–154Google Scholar
  5. Bittner M, Strejc J, Matoulkova D, Kolska Z, Pustelnikova T, Branyik T (2017) Adhesion of Megasphaera cerevisiae onto solid surfaces mimicking materials used in breweries. J I Brewing 123:204–210Google Scholar
  6. Bos R, van der Mei HC, Busscher HJ (1999) Physico-chemistry of initial microbial adhesive interactions-its mechanisms and methods for study. FEMS Microbiol Rev 23:179–230Google Scholar
  7. Chang SS, Kang DH (2004) Alicyclobacillus spp. in the fruit juice industry: history characteristics and current isolation, detection procedures. Crit Rev Microbiol 30:55–74Google Scholar
  8. Chen S, Tang Q, Zhang X, Zhao G, Hu X, Liao X, Chen F, Wu J, Xiang H (2006) Isolation and characterization of thermo-acidophilic endospore-forming bacteria from the concentrated apple juice-processing environment. Food Microbiol 23:439–445Google Scholar
  9. do Prado BD, Fernandes MD, dos Anjos MM, Tognim MCB, Nakamura CV, Machinski M, Mikcha JMG, de Abreu BA (2018) Biofilm-forming ability of Alicyclobacillus spp. isolates from orange juice concentrate processing plant. J Food Saf 38:e12466Google Scholar
  10. dos Anjos MM, Ruiz SP, Nakamura CV, de Abreu Filho BA (2013) Resistance of Alicyclobacillus acidoterrestris spores and biofilm to industrial sanitizers. J Food Protect 76:1408–1413Google Scholar
  11. Frank JF (2000) Control of biofilms in the food and beverage industry. In: Walker J, Surman S, Jass JH (eds) Industrial biofouling: detection, prevention and control. Wiley, Chichester, pp 205–224Google Scholar
  12. Gispert MP, Serro AP, Colaco R, Saramago B (2008) Bovine serum albumin adsorption onto 316L stainless steel and alumina: a comparative study using depletion, protein radiolabeling, quartz crystal microbalance and atomic force microscopy. Surf Interface Anal 40:1529–1537Google Scholar
  13. Hamouda T, Shih AY, Baker JR Jr (2002) A rapid staining technique for the detection of the initiation of germination of bacterial spores. Lett Appl Microbiol 34:86–90Google Scholar
  14. Huang XC, Yuan YH, Guo CF, Gekas V, Yue TL (2015a) Alicyclobacillus in the fruit juice industry: spoilage, detection, and prevention/control. Food Rev Int 31:91–124Google Scholar
  15. Huang Q, Yang Y, Hu R, Lin C, Sun L, Vogler EA (2015b) Reduced platelet adhesion and improved corrosion resistance of superhydrophobic TiO2-nanotube-coated 316L stainless steel. Colloid Surf B 125:134–141Google Scholar
  16. Israelachvili JN (2011) Intermolecular and surface forces. Academic Press, LondonGoogle Scholar
  17. McKnight IC, Eiroa MNU, Sant’Ana AS, Massaguer PR (2010) Alicyclobacillus acidoterrestris in pasteurized exotic Brazilian fruit juices: isolation, genotypic characterization and heat resistance. Food Microbiol 27:1016–1022Google Scholar
  18. Olszewska MA (2013) Microscopic findings for the study of biofilms in food environments. Acta Biochim Pol 60:531–537Google Scholar
  19. Peng JS, Tsai WC, Chou CC (2002) Inactivation and removal of Bacillus cereus by sanitizer and detergent. Int J Food Microbiol 77:11–18Google Scholar
  20. Pettipher GL, Osmundson M, Murphy J (1997) Methods for the detection and enumeration of Alicyclobacillus acidoterrestris and investigation of growth and production of taint in fruit juice and fruit juice-containing drinks. Lett Appl Microbiol 24:185–189Google Scholar
  21. Prochazkova G, Podolova N, Safarik I, Zachleder V, Branyik T (2013) Physicochemical approach to freshwater microalgae harvesting with magnetic particles. Colloid Surf B 112:213–218Google Scholar
  22. Redman JA, Walker SL, Elimelech M (2004) Bacterial adhesion and transport in porous media: role of the secondary energy minimum. Environ Sci Technol 38:1777–1785Google Scholar
  23. Sauer K (2003) The genomics and proteomics of biofilm formation. Genome Biol 4:219Google Scholar
  24. Sharma PK, Hanumantha Rao K (2002) Analysis of different approaches for evaluation of surface energy of microbial cells by contact angle goniometry. Adv Colloid Interfac 98:341–463Google Scholar
  25. Shemesh M, Pasvolsky R, Zakin V (2014) External pH is a cue for the behavioral switch that determines surface motility and biofilm formation of Alicyclobacillus acidoterrestris. J Food Prot 77:1418–1423Google Scholar
  26. Smit Y, Cameron M, Venter P, Witthuhn RC (2011) Alicyclobacillus spoilage and isolation—a review. Food Microbiol 28:331–349Google Scholar
  27. Spinelli ACNF, Sant’Ana AS, Pacheco-Sanchez CP, Massaguer PR (2010) Influence of the hot-fill water-spray-cooling process after continuous pasteurization on the number of decimal reductions and on Alicyclobacillus acidoterrestris CRA 7152 growth in orange juice stored at 35 °C. Int J Food Microbiol 137:295–298Google Scholar
  28. Srey S, Jahid IK, Ha SD (2013) Biofilm formation in food industries: a food safety concern. Food Control 31:572–585Google Scholar
  29. Steyn CE, Cameron M, Witthuhn RC (2011) Occurrence of Alicyclobacillus in the fruit processing environment—a review. Int J Food Microbiol 147:1–11Google Scholar
  30. Storgards E, Tapani K, Hartwall P, Saleva R, Suihko ML (2006) Microbial attachment and biofilm formation in brewery bottling plants. J Am Soc Brew Chem 64:8–15Google Scholar
  31. Tianli Y, Jiangbo Z, Yahong Y (2014) Spoilage by Alicyclobacillus bacteria in juice and beverage products: chemical, physical, and combined control methods. Compr Rev Food Sci F 13:771–797Google Scholar
  32. Tyfa A, Kunicka-Styczynska A, Zabielska J (2015) Evaluation of hydrophobicity and quantitative analysis of biofilm formation by Alicyclobacillus sp. Acta Biochim Pol 62:785–790Google Scholar
  33. van Oss CJ (1995) Hydrophobicity of biosurfaces–origin, quantitative determination and interaction energies. Colloid Surf B 5:91–110Google Scholar
  34. van Oss CJ (2003) Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. J Mol Recognit 16:177–190Google Scholar
  35. van Oss CJ (2006) Interfacial forces in aqueous media. CRC Press, Boca RatonGoogle Scholar

Copyright information

© Springer Japan KK, part of Springer Nature 2019

Authors and Affiliations

  • Jan Strejc
    • 1
  • Lucie Kyselova
    • 1
  • Anna Cadkova
    • 1
  • Tomas Potocar
    • 1
  • Tomas Branyik
    • 1
    Email author
  1. 1.Department of BiotechnologyUniversity of Chemistry and Technology PraguePragueCzech Republic

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