Abstract
The influence of the physicochemical properties of biomaterials on microbial cell adhesion is well known, with the extent of adhesion depending on hydrophobicity, surface charge, specific functional groups and acid–base properties. Regarding yeasts, the effect of cell surfaces is often overlooked, despite the fact that generalisations may not be made between closely related strains. The current investigation compared adhesion of three industrially relevant strains of Saccharomyces cerevisiae (M-type, NCYC 1681 and ALY, strains used in production of Scotch whisky, ale and lager, respectively) to the biomaterial hydroxylapatite (HAP). Adhesion of the whisky yeast was greatest, followed by the ale strain, while adhesion of the lager strain was approximately 10-times less. According to microbial adhesion to solvents (MATS) analysis, the ale strain was hydrophobic while the whisky and lager strains were moderately hydrophilic. This contrasted with analyses of water contact angles where all strains were characterised as hydrophilic. All yeast strains were electron donating, with low electron accepting potential, as indicated by both surface energy and MATS analysis. Overall, there was a linear correlation between adhesion to HAP and the overall surface free energy of the yeasts. This is the first time that the relationship between yeast cell surface energy and adherence to a biomaterial has been described.
Similar content being viewed by others
References
Alsteens D, Dupres V, Mc Evoy K, Wildling L, Gruber HJ, Dufrêne YF (2008) Structure, cell wall elasticity and polysaccharide properties of living yeast cells, as probed by AFM. Nanotechnology. doi:10.1088/0957-4484/19/38/384005
Aronov D, Chaikina M, Haddad J, Karlov A, Mezinskis G, Oster L, Pavlovska I, Rosenman G (2007) Electronic states spectroscopy of hydroxyapatite ceramics. J Mater Sci Mater Med 18:865–870
Baillez S, Nzihou A, Bernache-Assolant D, Champion E, Sharrock P (2007) Removal of aqueous lead ions by hydroxyapatite: equilibria and kinetic processes. J Hazard Mater A139:443–446
Baptista CMSG, Cóias JMA, Oliveira ACM, Oliveira NMC, Rocha JMS, Dempsey MJ, Lannigan KC, Benson PS (2006) Natural immobilisation of microorganisms for continuous ethanol production. Enzym Microb Technol 40:127–131
Bellon-Fontaine M-N, Rault J, Van Oss CJ (1996) Microbial adhesion to solvents: a novel method to determine the electron-donor/electron-acceptor or Lewis acid–base properties of microbial cells. Colloids Surf B 7:47–53
Bertazzo S, Zambuzzi WF, Campos DDP, Ogeda TL, Ferreira CV, Bertran CA (2010) Hydroxyapatite surface solubility and effect on cell adhesion. Colloid Surf B 78:177–184
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 23:179–229
Brányik T, Vicente A, Oliveira R, Teixeira J (2004) Physicochemical surface properties of brewing yeast influencing their immobilization onto spent grains in a continuous reactor. Biotechnol Bioeng 88:84–93
Demuyakor B, Ohta Y (1992) Promotive action of ceramics on yeast ethanol and production and its relationship to pH, glycerol and alcohol dehydrogenase activity. Appl Microbiol Biotechnol 36:717–721
Dengis PB, Rouxhet PG (1997) Surface properties of top- and bottom-fermenting yeast. Yeast 13:931–943
Dragone G, Mussatto SI, Almeida e Silva JB (2008) Influence of temperature on continuous high gravity brewing with yeasts immobilized on spent grains. Eur Food Res Technol 228:257–264
Gómez del Río JA, Morando PJ, Cicerone DS (2004) Natural materials for treatment of industrial effluents: comparative study of the retention of Cd, Zn and Co by calcite and hydroxyapatite. Part I: Batch experiments. J Environ Manag 71:169–177
Gross KA, Berndt CC (2002) Biomedical applications of apatites. In: Kohn MJ, Rakovan J, Hughes JM (eds) Rev mineral geochem, vol 48. Mineralogical Society of America, Washington, DC, pp 631–672
Guillemot G, Vaca-Medina G, Martine-Yken H, Vernhet A, Schmitz P, Mercier-Bonin M (2006) Shear-flow induced detachment of Saccharomyces cerevisiae from stainless steel: influence of yeast and solid-surface properties. Colloid Surf B 49:126–135
Henriques M, Azeredo J, Oliveira R (2004) Adhesion of Candida albicans and Candida dubliniensis to acrylic and hydroxyapatite. Colloid Surf B 33:235–241
Itoh S, Nakamura S, Nakamura M, Shinomiya K, Yamashita K (2006) Enhanced bone ingrowth into hydroxyapatite with interconnected pores by electrical polarization. Biomaterials 27:5572–5579
Kandori K, Masunari A, Ishikawa T (2005) Study on adsorption mechanism of proteins onto synthetic calcium hydroxyapatites through ionic concentration measurements. Calcif Tissue Int 76:194–206
Kang S, Choi H (2005) Effect of surface hydrophobicity on the adhesion of S. cerevisiae onto modified surfaces by poly(styrene-ran-sulfonic acid) random copolymers. Colloid Surf B 46:70–77
Kinnari TJ, Esteban J, Martin-de-Hijas NZ, Sánchez-Muñoz O, Sánchez-Salcedo S, Colilla M, Vallet-Regí M, Gomez-Barrena E (2009) Influence of surface porosity and pH on bacterial adherence to hydroxyapatite and biphasic calcium phosphate bioceramics. J Med Microbiol 58:132–137
Kojic EM, Darouiche RO (2004) Candida infections of medical devices. Clin Microbiol Rev 17:255–267
Kourkoutas Y, Bekatorou A, Koutinas AA, Banat IM, Marchant R (2004) Immobilization technologies and support materials suitable in alcohol beverages production: a review. Food Microbiol 21:377–397
Liu Y, Zhao Q (2005) Influence of surface energy of modified surfaces on bacterial adhesion. Biophys Chem 117:39–45
Misra V, Chaturvedi PK (2007) Plant uptake/bioavailability of heavy metals from the contaminated soil after treatment with humus soil and hydroxyapatite. Environ Monit Assess 133:169–176
Mortensen HD, Gori K, Jespersen L, Arneborg N (2005) Debaryomyces hansenii strains with different cell sizes and surface physicochemical properties adhere differently to a solid agarose surface. FEMS Microbiol Lett 249:165–170
Nakari-Setälä T, Azeredo J, Henriques M, Oliveira R, Teixeira J, Linder M, Penttilä M (2002) Expression of a fungal hydrophobin in the Saccharomyces cerevisiae cell wall: effect on cell surface properties and immobilization. Appl Environ Microbiol 68:3385–3391
Ong JL, Chan DCN (2000) Hydroxyapatite and their use as coatings in dental implants: a review. Crit Rev Biomed Eng 28:667A–707A
Pereira-Cenci T, Deng DM, Kraneveld EA, Manders EM, Del Bel Cury AA, Ten Cate JM, Crielaard W (2008) The effect of Streptococcus mutans and Candida glabrata on Candida albicans biofilms formed on different surfaces. Arch Oral Biol 53:755–764
Powell CD, Quain DE, Smart KA (2003) The impact of brewing yeast cell age on fermentation performance, attenuation and flocculation. FEMS Yeast Res 3:149–157
Tata M, Bower P, Bromberg S, Duncombe D, Fehring J, Lau V, Ryder D, Stassi P (1999) Immobilized yeast bioreactor systems for continuous beer fermentation. Biotechnol Prog 15:105–113
Van Der Mei HC, Bos R, Busscher HJ (1998) A reference guide to microbial cell surface hydrophobicity based on contact angles. Colloid Surf B 11:213–221
Van Oss CJ (1995) Hydrophobicity of biosurfaces—origin, quantitative determination and interaction energies. Colloid Surf B 5:91–110
Van Oss CJ, Good RJ, Chaudhary MK (1986) The role of van der Waals forces and hydrogen bonds in ‘hydrophobic interactions’ between biopolymers and low energy surfaces. J Colloid Interface Sci 111:378–390
Van Oss CJ, Good RJ, Chaudhary MK (1988) Additive and non-additive surface tension components and the interpretation of contact angles. Langmuir 4:884–891
Verbelen PJ, De Shutter DP, Delvaux F, Verstrepen KJ, Delvaux FR (2006) Immobilized yeast cell systems for continuous fermentation applications. Biotechnol Lett 28:1515–1525
Vernhet A, Bellon-Fontaine MN (1995) Role of bentonites in the prevention of Saccharomyces cerevisiae adhesion to solid surfaces. Colloid Surf B 3:255–262
Verstrepen KJ, Derdelinckx G, Verachtert H, Delvaux FR (2003) Yeast flocculation: what brewers should know. Appl Microbiol Biotechnol 61:197–205
Zhao Q, Liu Y, Wang C, Wang S, Müller-Steinhagen H (2005) Effect of surface free energy on the adhesion of biofouling and crystalline fouling. Chem Eng Sci 60:4858–4865
Acknowledgments
This work was funded by European Commission Project NMP3-CT-504937 ‘PERCERAMICS’. The authors wish to thank Yun Liu and Qi Zhao, Division of Mechanical Engineering and Mechatronics, University of Dundee, Scotland for the contact angle measurements and surface energy calculations. The authors are grateful to the Institute of Silica Materials, Riga Technical University, Latvia for fabricating and supplying the HAP tablets.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
White, J.S., Walker, G.M. Influence of cell surface characteristics on adhesion of Saccharomyces cerevisiae to the biomaterial hydroxylapatite. Antonie van Leeuwenhoek 99, 201–209 (2011). https://doi.org/10.1007/s10482-010-9477-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10482-010-9477-6