Skip to main content

Physicochemical aspects of Trichosporon cutaneum CCY 30-5-10 adhesion and biofilm formation potential on cellophane

Abstract

This paper focuses on the adhesion and biofilm formation potential of cellulolytic yeast Trichosporon cutaneum CCY 30-5-10 on solid cellophane from a novel perspective. First, physicochemical characterisation of the cells and carrier (cellophane) was performed to evaluate the effect of different culture media (complex vs mineral) on yeast cell adhesion. (Un)favourable adhesion conditions were predicted using the thermodynamic approach. Next, the ability of the cells to colonise the carrier under the above conditions was quantified and the biofilm structure was characterised using image analysis. The approaches described were found suitable to predict and experimentally verify favourable (cell-solid) adhesion, i.e. the hydrophobic and low electron-donor nature of cellophane together with hydrophobic cells (obtained when cultivated in a complex culture medium) were found to have a major impact in defining successful yeast adhesion with subsequent biofilm formation.

This is a preview of subscription content, access via your institution.

References

  1. Alonso, A. N., Pomposiello, P. J., & Leschine, S. B. (2008) Biofilm formation in the life cycle of the cellulolytic actinomycete Thermobifida fusca. Biofilms, 2008, 1–11. DOI: 10.1017/s1479050508002238.

    Article  Google Scholar 

  2. Beyenal, H., Donovan, C., Lewandowski, Z., & Harkin, G. (2004) Three-dimensional biofilm structure quantification. Journal of Microbiological Methods, 59, 395–413. DOI: 10.1016/j.mimet.2004.08.003.

    CAS  Article  Google Scholar 

  3. Bos, R., van der Mei, H. C., & Busscher, H. J. (1999) Physicochemistry of initial microbial adhesive interactions — its mechanisms and methods for study. FEMS Microbiology Reviews, 23, 179–230. DOI: 10.1111/j.1574-6976.1999.tb00396.x.

    CAS  Article  Google Scholar 

  4. Bruinsma, G. M., van der Mei, H. C., & Busscher, H. (2001) Bacterial adhesion to surface hydrophilic and hydrophobic contact lenses. Biomaterials, 22, 3217–3224. DOI: 10.1016/s0142-9612(01)00159-4.

    CAS  Article  Google Scholar 

  5. Cerca, N., Pier, G. B., Vilanova, M., Oliveira, R., & Azeredo, J. (2005) Quantitative analysis of adhesion and biofilm formation on hydrophilic and hydrophobic surfaces of clinical isolates of Staphylococcus epidermidis. Research of Microbiology, 156, 506–514. DOI: 10.1016/j.resmic.2005.01.007.

    CAS  Article  Google Scholar 

  6. Cunliffe, D., Smart, C. A., Alexander, C., & Vulfson, E. N. (1999) Bacterial adhesion at synthetic surfaces. Applied and Environment Microbiology, 65, 4995–5002.

    CAS  Google Scholar 

  7. Dennis, C. (1972) Breakdown of cellulose by yeast species. Journal of General Microbiology, 71, 409–411. DOI: 10.1099/00221287-71-2-409.

    Article  Google Scholar 

  8. Di Bonaventura, G., Pompilio, A., Picciani, C., Iezzi, M., D’Antonio, D., & Piccolomini, R. (2006) Biofilm formation by the emerging fungal pathogen Trichosporon asahii: Development, architecture, and antifungal resistance. Antimicrobial Agents and Chemotherapy, 50, 269–3276. DOI: 10.1128/aac.00556-06.

    Article  Google Scholar 

  9. Dufrene, Y. F., & Rouxhet, P. G. (1996) X-ray photoelectron spectroscopy analysis of the surface composition of Azospirillum brasilense in relation to growth conditions. Colloids and Surfaces B: Biointerfaces, 7, 271–279. DOI: 10.1016/0927-7765(96)01295-7.

    CAS  Article  Google Scholar 

  10. Dunne, W. M., Jr., (2002) Bacterial adhesion: Seen any good biofilms lately? Clinical Microbiology Reviews, 15, 155–166. DOI: 10.1128/cmr.2.155-166.2002.

    CAS  Article  Google Scholar 

  11. Fonseca, F. L., Frases, S., Casadevall, A., Fischman-Gompertz, O., Nimrichter, L., & Rodrigues, M. L. (2009) Structural and functional properties of the Trichosporon asahii glucuronoxylomannan. Fungal Genetics and Biology, 46, 496–505. DOI: 10.1016/j.fgb.2009.03.003.

    CAS  Article  Google Scholar 

  12. Georgieva, N., Yotova, L., Betcheva, R., Hadzhiyska, H., & Valtchev, I. (2006) Biobleaching of lignin in linen by degradation with Trichosporon cutaneum R57. Journal of the University of Chemical Technology and Metallurgy, Sofia, 41, 153–156.

    CAS  Google Scholar 

  13. Gusakov, A. V. (2011) Alternatives to Trichoderma reesei in biofuel production. Trends in Biotechnology, 29, 419–425. DOI: 10.1016/j.tibtech.2011.04.004.

    CAS  Article  Google Scholar 

  14. Hamadi, F., & Latrache, H. (2008) Comparison of contact angle measurement and microbial adhesion to solvents for assaying electron donor-electron acceptor (acid-base) properties of bacterial surface. Colloids and Surfaces B: Biointerfaces, 65, 134–139. DOI: 10.1016/j.colsurfb.2008.03.010.

    CAS  Article  Google Scholar 

  15. Hrmová, M., Biely, P., Vršanská, M., & Petráková, E. (1984) Induction of cellulose- and xylan-degrading enzyme complex in the yeast Trichosporon cutaneum. Archives of Microbiology, 138, 371–376. DOI: 10.1007/bf00410906.

    Article  Google Scholar 

  16. Ichikawa, T., Nishikawa, A., Wada, H., Ikeda, R., & Shinoda, T. (2001) Structural studies of the antigen III cell wall polysaccharide of Trichosporon domesticum. Carbohydrate Research, 330, 495–503. DOI: 10.1016/s0008-6215(00)00325-6.

    CAS  Article  Google Scholar 

  17. Jackson, G., Beyenal, H., Rees, W. M., & Lewandowski, Z. (2001) Growing reproducible biofilms with respect to structure and viable cell counts. Journal of Microbiological Methods, 47, 1–10. DOI: 10.1016/s0167-7012(01)00280-9.

    CAS  Article  Google Scholar 

  18. Jana, T. K., Srivastava, A. K., Csery, K., & Arora, D. K. (2000) Influence of growth and environmental conditions on cell surface hydrophobicity of Pseudomonas fluorescens in non-specific adhesion. Canadian Journal of Microbiology, 46, 28–37. DOI: 10.1139/w99-104.

    CAS  Article  Google Scholar 

  19. Kausar, H., Sariah, M., Mohd Saud, H., Zahangir Alam, M., & Razi Ismail, M. (2011) Isolation and screening of potential actinobacteria for rapid composting of rice straw. Biodegradation, 22, 367–375. DOI: 10.1007/s10532-010-9407-3.

    CAS  Article  Google Scholar 

  20. Kuřec, M., & Brányik, T. (2011) The role of physicochemical interactions and FLO genes expression in the immobilization of industrially important yeasts by adhesion. Colloids and Surfaces B: Biointerfaces, 84, 491–497. DOI: 10.1016/j.colsurfb.2011.02.004.

    Article  Google Scholar 

  21. Lewandowski, Z., & Beyenal, H. (2007) Fundamentals of biofilm research. Boca Raton, FL, USA: CRC Press.

    Book  Google Scholar 

  22. Liu, Y., & Tay, J. H. (2002) The essential role of hydrodynamic shear force in the formation of biofilm and granular sludge. Water Research, 36, 1653–1665. DOI: 10.1016/s0043-1354(01)00379-7.

    CAS  Article  Google Scholar 

  23. Lynd, L. R., Weimer, P. J., van Zyl, W. H., & Pretorius, I. S. (2002) Microbial cellulose utilization: Fundamentals and biotechnology. Microbiology and Molecular Biology Research, 66, 506–577. DOI: 10.1128/mmbr.66.3.506-577.2002.

    CAS  Article  Google Scholar 

  24. Lynd, L. R., Weimer, P. J., Wolfaardt, G., & Zhang, Y. H. (2006) Cellulose hydrolysis by Clostridium thermocellum: A microbial perspective. In V. Uversky, & I. A. Kataeva (Eds.), Cellulosome: Molecular anatomy and physiology of proteinaceous machines (pp. 95–117). New York, NY, USA: Nova Science Publishers.

    Google Scholar 

  25. Mercier-Bonin, M., Ouazzani, K., Schmitz, P., & Lorthois, S. (2004) Study of bioadhesion on a flat plate with a yeast/glass model system. Journal of Colloid and Interface Science, 271, 342–350. DOI: 10.1016/j.jcis.2003.11.045.

    CAS  Article  Google Scholar 

  26. Miron, J., & Forsberg, C. (1999) Characterization of cellulose-binding proteins that are involved in adhension mechanism of Fibrobacter intestinalis DR7. Applied Microbiology and Biotechnology, 51, 491–497. DOI: 10.1007/s002530051422.

    CAS  Article  Google Scholar 

  27. Miron, J., Ben-Ghedalla, D., & Morrison, M. (2001) Invited review: Adhesion mechanisms of rumen cellulolytic bacteria. Journal of Dairy Science, 84, 1294–1309. DOI: 10.3168/jds.s0022-0302(01)70159-2.

    CAS  Article  Google Scholar 

  28. Mohamed, N., Teeters, M.A., Patti, J.M., Höök, M., & Ross, J. M. (1999) Inhibition of Staphylococcus aureus adherence to collagen under dynamic conditions. Infection and Immunity, 67, 589–594.

    CAS  Google Scholar 

  29. Morrison, M., & Miron, J. (2000) Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and and Pil-proteins? FEMS Microbiol Letters, 185, 109–115. DOI: 10.1111/j.1574-6968.2000.tb09047.x.

    CAS  Article  Google Scholar 

  30. Paul, E., Ochoa, J. C., Pechaud, Y., Liu, Y., & Liné, A. (2012) Effect of shear stress and growth conditions on detachment and physical properties of biofilms. Water Research, 46, 5499–5508. DOI: 10.1016/j.watres.2012.07.029.

    CAS  Article  Google Scholar 

  31. Rouxhet, P. G., Mozes, N., Dengis, P. B., Dufręne, Y. F., Gerin, P. A., & Genet, M. J. (1994) Application of x-ray photoelectron spectroscopy to microorganisms. Colloids and Surfaces B: Biointerfaces, 2, 347–369. DOI: 10.1016/0927-7765(94)80049-9.

    CAS  Article  Google Scholar 

  32. Sadhu, S., & Maiti, T. K. (2013) Cellulase production by bacteria: A review. British Microbiology Research Journal, 3, 235–258. DOI: 10.9734/bmrj/2013/2367.

    CAS  Article  Google Scholar 

  33. Sharma, P. K., & Rao, K. H. (2002) Analysis of different approaches for evaluation of surface energy of microbial cells by contact angle goniometry. Advances in Colloid and Interface Science, 98, 341–463. DOI: 10.1016/s0001-8686(02)00004-0.

    CAS  Article  Google Scholar 

  34. Shi, Z. J., Luo, G. S., & Wang, G. J. (2012) Cellulomonas carbonis sp. nov., isolated from coal mine soil. International Journal of Systematic Evolutionary Microbiology, 62, 2004–2010. DOI: 10.1099/ijs.0.034934-0.

    CAS  Article  Google Scholar 

  35. Shoham, Y., Lamed, R., & Bayer, E. A. (1999) The cellulosome concept as an efficient microbial strategy for the degradation of insoluble polysaccharides. Trends in Microbiology, 7, 275–281. DOI: 10.1016/s0966-842x(99)01533-4.

    CAS  Article  Google Scholar 

  36. Sirmerova, M., Prochazkova, G., Siristova, L., Kolska, Z., & Branyik, T. (2013) Adhesion of Chlorella vulgaris to solid surfaces, as mediated by physicochemical interactions. Journal of Applied Phycology, 25, 1687–1695. DOI: 10.1007/s10811-013-0015-6.

    CAS  Article  Google Scholar 

  37. Song, H. H., Clarke, W. P., & Blackall, L. L. (2005) Concurrent microscopic observations and activity measurements of cellulose hydrolyzing and methanogenic populations during the batch anaerobic digestion of crystalline cellulose. Biotechnology and Bioengineering, 91, 369–378. DOI: 10.1002/bit.20517.

    CAS  Article  Google Scholar 

  38. Song, N., Cai, H. Y., Yan, Z. S., & Jiang, H. L. (2013) Cellulose degradation by one mesophilic strain Caulobacter sp. FMC1 under both aerobic and anaerobic conditions. Bioresource Technology, 131, 281–287. DOI: 10.1016/j.biortech.2013.01.003.

    CAS  Article  Google Scholar 

  39. van Loosdrecht, M.C.M., Heijnen, J.J., Eberl, H., Kreft, J., & Picioreanu, C. (2002) Mathematical modelling of biofilm structures. Antonie van Leeuwenhoek, 81, 245–256. DOI: 10.1023/a:1020527020464.

    Article  Google Scholar 

  40. van Oss, C. J. (1995) Hydrophobicity of biosurfaces — origin, quantitative determination and interaction energies. Colloids and Surfaces B: Biointerfaces, 5, 91–110. DOI: 10.1016/0927-7765(95)01217-7.

    Article  Google Scholar 

  41. van Oss, C. J. (2003) Long-range and short-range mechanisms of hydrophobic attraction and hydrophilic repulsion in specific and aspecific interactions. Journal of Molecular Recognition, 16, 177–190. DOI: 10.1002/jmr.618.

    Article  Google Scholar 

  42. Wang, Z. W., & Chen, S. L. (2009) Potential of biofilm-based biofuel production. Applied Microbiology and Biotechnology, 83, 1–18. DOI: 10.1007/s00253-009-1940-9.

    CAS  Article  Google Scholar 

  43. Wang, Z. W., Lee, S. H., Elkins, J. G., & Morrell-Falvey, J. L. (2011) Spatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum. AMB Express, 1, 30. DOI: 10.1186/2191-0855-1-30.

    Article  Google Scholar 

  44. Wenzel, M., Schönig, I., Berchtold, M., Kämpfer, P., & König, H. (2002) Aerobic and facultatively anaerobic cellulolytic bacteria form the gut of the termite Zootermopsis angusticollis. Journal of Applied Microbiology, 92, 32–40. DOI: 10.1046/j.1365-2672.2002.01502.x.

    CAS  Article  Google Scholar 

  45. Yang, X. M., Beyenal, H., Harkin, G., & Lewandowski, Z. (2000) Quantifying biofilm structure using image analysis. Journal of Microbiological Methods, 39, 109–119. DOI: 10.1016/s0167-7012(99)00097-4.

    CAS  Article  Google Scholar 

  46. Young, J. M., Leschine, S. B., & Reguera, G. (2012) Reversible control of biofilm formation by Cellulomonas spp. in response to nitrogen availability. Environmental Microbiology, 14, 594–604. DOI: 10.1111/j.1462-2920.2011.02596.x.

    CAS  Article  Google Scholar 

  47. Zhong, L. J., Pang, L. Q., Che, L. M., Wu, X. E., & Chen, X. D. (2013) Nafion coated stainless steel for anti-biofilm application. Colloids and Surfaces B: Biointerfaces, 111, 252–256. DOI: 10.1016/j.colsurfb.2013.05.039.

    CAS  Article  Google Scholar 

Download references

Author information

Affiliations

Authors

Corresponding author

Correspondence to Tomáš Brányik.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Dostálková, J., Procházková, G., Jirků, V. et al. Physicochemical aspects of Trichosporon cutaneum CCY 30-5-10 adhesion and biofilm formation potential on cellophane. Chem. Pap. 69, 425–432 (2015). https://doi.org/10.1515/chempap-2015-0046

Download citation

Keywords

  • cellophane
  • Trichosporon cutaneum
  • biofilm formation
  • adhesion
  • physicochemical surface characterisation
  • thermodynamic model