Abstract
Fungal surface hydrophobicity is involved in several functions in fungal growth and development. Water contact angles measurement has been used as a direct and simple approach for its characterisation in solid cultures. Microsphere adhesion assay is said to be the best method to assess cell hydrophobicity of filamentous fungi. This study aimed to apply these two methods to study hydrophobicity of Penicillium expansum and Penicillium brevicompactum grown as mycelial mats in solid culture, liquid culture and water biofilms. As result, both species in solid cultures were classified as hydrophobic with contact angles ≥90º, but in liquid cultures and water biofilms showed different levels of hydrophobicity when microsphere adhesion assay was applied. In addition, was found that biofilms have specific hydrophobic hyphae which may be involved in fungal ecological functions.
Similar content being viewed by others
References
Amiri A, Cholodowski D, Bompeix G (2005) Adhesion and germination of waterborne and airborne conidia of Penicillium expansum to apple and inert surfaces. Physiol Mol Plant Path 67:40–48
Baschien C, Rode G, Böckelmann U, Götz P, Szewzyk U (2009) Interactions between hyphosphere-associated bacteria and the fungus Cladosporium herbarum on aquatic leaf litter. Microb Ecol 58:642–650
Beauvais A, Schmidt C, Guadagnini S, Roux P, Perret E, Henry C, Paris S, Mallet A, Prévost M-C, Latgé JP (2007) An extracellular matrix glues together the aerial-grown hyphae of Aspergillus fumigatus. Cell Microbiol 9:1588–1600
Braganra SM, Azevedo NF, Simoes LC, Keevil CW, Vieira MJ (2007) Use of fluorescent in situ hybridisation for the visualisation of Helicobacter pylori in real drinking water biofilms. Water Sci Technol 55:387–393
Busscher HJ, Van Pelt AWJ, de Boer P, de Jong HP, Arends J (1984) The effect of surface roughening of polymers on measured contact angles of liquids. Colloid Surf Physicochem Eng Aspect 9:319–331
Chandra J, Patel JD, Jian L, Zhou G, Mukherjee PK, McCormick TS, Anderson JM, Ghannoum MA (2005) Modification of surface properties of biomaterials influences the ability of Candida albicans to form biofilms. Appl Environ Microbiol 71:8795–8801
Chau HW, Si BC, Goh YK, Vujanovic V (2009) A novel method for identifying hydrophobicity on fungal surfaces. Mycol Res 43:117–126
Chau HW, Goh YK, Si BC, Vujanovic V (2010) Assessment of alcohol percentage test for fungal surface hydrophobicity measurement. Lett Appl Microbiol 50:295–300
de Boer W, Klein PJA, Kowalchuk GA, Van Veen JA (2001) Growth of chitinolytic dune soil β-subclass proteobacteria in response to invading fungal hyphae. Appl Environ Microbiol 67:3358–3362
de Boer WJH, Leveau J, Kowalchuk GA, Klein PJA, Abeln ECA, Figge MJ, Sjollema K, Janse JD, van Veen JA (2004) Collimonas fungivorans gen. nov., sp. nov., a chitinolytic soil bacterium with the ability to grow on living fungal hyphae. Int J Syst Evol Microbiol 54:857–864
de Boer W, Folman LB, Summerbell RC, Boddy L (2005) Living in a fungal world: impact of fungi on soil bacterial niche development. FEMS Microbiol Rev 29:795–811
Donlan R, Costerton JW (2002) Biofilms: survival mechanisms of clinically relevant microorganisms. Clin Microbiol Rev 15:167–193
Doyle R, Rosenberg M (1990) Microbial cell surface hydrophobicity: history, measurement, and significance. In: Doyle R, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, pp 1–37
Doyle RJ (2000) Contribution of the hydrophobic effect to microbial infection. Microb Infect 2:391–400
Elvers KT, Leeming K, Lappin-Scott HM (2002) Binary and mixed population biofilms: time-lapse image analysis and disinfection with biocides. J Ind Microbiol Biotechnol 29:331–338
Epstein AK, Pokroy B, Seminara A, Aizenberg J (2011) Bacterial biofilm shows persistent resistance to liquid wetting and gas penetration. PNAS 108:995–1000
Gonçalves AB, Paterson RRM, Lima N (2006) Survey and significance of filamentous fungi from tap water. Int J Hyg Environ Health 209:257–264
Hageskal G, Lima N, Skaar I (2009) The study of fungi in drinking water. Mycol Res 113:165–172
Hazen KC (1990) Cell surface hydrophobicity of medically important fungi especially Candida species. In: Doyle R, Rosenberg M (eds) Microbial cell surface hydrophobicity. American Society for Microbiology, Washington, pp 249–295
Hazen KC, Hazen BW (1987) A polystyrene microsphere assay for detecting surface hydrophobicity variations within Candida albicans populations. J Immunol Methods 6:289–299
Henriques M, Azeredo J, Oliveira R (2004) Adhesion of Candida albicans and Candida dubliniensis to acrylic and hydroxyapatite. Colloids Surf B 33:235–241
Hoffman MT, Arnold AE (2010) Diverse bacteria inhabit living hyphae of phylogenetically diverse fungal endophytes. Appl Environ Microbiol 76:4063–4075
Hogan DA, Wargo MJ, Beck N (2007) Bacterial biofilms on fungal surfaces. In: Kjellebergue S, Giviskov M (eds) The biofilm mode of life. Horizons Biosciences, Wymondham
Howard FJ, Douglas LJ (2002) Interactions between Candida species and bacteria in mixed infections. In: Brogden KA, Guthmiller JM (eds) Polymicrobial diseases. ASM Press, Washington
Li F, Palecek SP (2008) Distinct domains of the Candida albicans adhesin Eap1p mediate cell–cell and cell-substrate interactions. Microbiology 154:1193–1203
Linder MB, Szilvay GR, Nakari-Setälä T, Penttila ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896
Mazumder S, Falkinham JO III, Dietrich AM, Puri IK (2010) Role of hydrophobicity in bacterial adherence to carbon nanostructures and biofilm formation. Biofouling 26:333–339
Morales DK, Hogan DA (2010) Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathogens. doi:10.1371/journal.ppat.1000886
Pascual S, de Cal A, Magan N, Melgarejo P (2000) Surface hydrophobicity, viability and efficacy in biological control of Penicillium oxalicum spores produced in aerial and submerged culture. J Appl Microbiol 89:847–853
Paterson RRM, Lima N (2005) Fungal contamination of drinking water. In: Lehr J, Keeley J, Lehr J, Kingery TB III (eds) Water encyclopedia. Wiley, Inc., Hoboken
Sammon NB, Harrower KM, Fabbro LD, Reed RH (2011) Three potential sources of microfungi in a treated municipal water supply system in sub-tropical Australia. Int J Environ Res Public Health 8:713–732
Simões M, Simões LC, Vieira MJ (2010) A review of current and emergent biofilm control strategies. LWT Food Sci Technol 43:573–583
Siqueira VM, Lima N (2011) Efficacy of free chlorine against water biofilms and spores of Penicillium brevicompactum. In: Ulrich Borchers, Clive Thompson K (ed) Water contamination emergencies: monitoring, understanding and acting. RSC Publishing, Cambridge, pp 157–165
Siqueira VM, Oliveira HMB, Santos C, Paterson RRM, Gusmão NB, Lima N (2011) Filamentous fungi in drinking water, particularly in relation to biofilm formation. Int J Environ Res Public Health 8:456–469
Smits THM, Wick L, Harms H, Keel C (2003) Characterization of the surface hydrophobicity of filamentous fungi. Environ Microbiol 5:85–91
Valdivia RH, Heitman J (2007) Endosymbiosis: the evil within. Curr Biol 17:408–410
Villena GK, Fujikawa T, Tsuyumu S, Gutiérrez-Correa M (2009) Structural analysis of biofilms and pellets of Aspergillus niger by confocal laser scanning microscopy and cryo scanning electron microscopy. Bioresource Technol 101:1920–1926
Watson CL, Owen RJ, Said B, Lai S, Lee JV, Surman-Lee S, Nichols G (2004) Detection of Helicobacter pylori by PCR but not culture in water and biofilm samples from drinking water distribution systems in England. J Appl Microbiol 97:690–698
Wessels JGH, de Vries OMH, Asgeirsdottir SA, Schuren FHJ (1991) Hydrophobin genes involved in formation of aerial hyphae and fruit bodies in Schizophyllum. Plant Cell 3:793–799
Wessels JGH (1997) Hydrophobins, proteins that change the nature of the fungal surface. Adv Microb Physiol 38:1–45
Whiteford JR, Spanu PD (2002) Hydrophobins and the interactions between fungi and plants. Mol Plant Path 3:391–400
Wimpenny J, Manz W, Szewzyk U (2000) Heterogeneity in biofilms. FEMS Microbiol Rev 24:661–671
Wingender J, Flemming H-C (2011) Biofilms in drinking water and their role as reservoir for pathogens. Int J Environ Res Public Health. doi:10.1016/j.ijheh.2011.05.009
Wösten HAB, Schuren FHJ, Wessels JGH (1994) Interfacial self-assembly of a hydrophobin into an amphipathic membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13:5848–5854
Wösten HAB, Willey JM (2000) Surface-active proteins enable microbial aerial hyphae to grow into the air. Microbiology 146:767–773
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Siqueira, V., Lima, N. Surface Hydrophobicity of Culture and Water Biofilm of Penicillium spp.. Curr Microbiol 64, 93–99 (2012). https://doi.org/10.1007/s00284-011-0037-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00284-011-0037-8