Advertisement

The Protein Journal

, Volume 34, Issue 4, pp 243–255 | Cite as

Recent Advances in Fungal Hydrophobin Towards Using in Industry

  • Mohammadreza KhalesiEmail author
  • Kurt Gebruers
  • Guy Derdelinckx
Article

Abstract

Fungal hydrophobin is a family of low molecular weight proteins consisting of four disulfide bridges and an extraordinary hydrophobic patch. The hydrophobic patch of hydrophobins and the molecules of gaseous CO2 may interact together and form the stable CO2-nanobubbles covered by an elastic membrane in carbonated beverages. The nanobubbles provide the required energy to provoke primary gushing. Due to the hydrophobicity of hydrophobin, this protein is used as a biosurfactant, foaming agent or encapsulating agent in food products and medicine formulations. Increasing demands for using of hydrophobins led to a challenge regarding production and purification of this product. However, the main issue to use hydrophobin in the industry is the regulatory affairs: yet there is no approved legislation for using hydrophobin in food and beverages. To comply with the legislation, establishing a consistent method for obtaining pure hydrophobins is necessary. Currently, few research teams in Europe are focusing on different aspects of hydrophobins. In this paper, an up-to-date collection of highlights from those special groups about the bio-chemical and physicochemical characteristics of hydrophobins have been studied. The recent advances of those groups concerning the production and purification, positive applications and negative function of hydrophobin are also summarised.

Keywords

Hydrophobin Production Purification Legislation Application Industry 

Abbreviations

EU

European Union

LMW

Low molecular weight

MW

Molecular weight

T. reesei

Trichoderma reesei

VTT Technical Research Centre

Valtion Teknillinen Tutkimuskeskus

Notes

Acknowledgments

The authors would like to thank the members of Hydrophobin Chair-Belgium for all their supports.

References

  1. 1.
    Cooper A, Kennedy MW (2010) Biofoams and natural protein surfactants. Biophys Chem 151:96–104Google Scholar
  2. 2.
    Deckers S, Vissers L, Gebruers K, Shokribousjein Z, Khalesi M, Riveros-Galan D, Schönberger C, Verachtert H, Neven H, Delcour J, Michiels C, Ilberg V, Derdelinckx G, Titze J, Martens J (2012) Doubly modified Carlsberg test combined with dynamic light scattering allows prediction of the primary gushing potential of harvested barley and malt. Cerevisia 37:77–81Google Scholar
  3. 3.
    Shokribousjein Z, Deckers SM, Gebruers K, Lorgouilloux Y, Baggerman G, Verachtert H, Delcour JA, Etienne P, Rock J-M, Michiels C, Derdelinckx G (2011) Hydrophobins, beer foaming and gushing. Cerevisia 35:85–101Google Scholar
  4. 4.
    Khalesi M, Deckers SM, Gebreurs K, Vissers L, Verachtert H, Derdenlickx G (2012) Hydrophobins: exceptional proteins for many applications in brewery environment and other bio-industries. Cerevisia 37:3–9Google Scholar
  5. 5.
    Khalesi M, Mandelings N, Shokribousjein Z, Riveros-Galan D, Verachtert H, Gebruers K, Delvigne F, Vankelecom I, Derdelinckx G (2014) Biophysical characterisation of hydrophobin enriched foamate. Cerevisia 38:129–134Google Scholar
  6. 6.
    Subkowski T, Karos M, Subkowski T (2007) Industrial performance proteins: hydrophobin-learning from nature. J Biotechnol 131:212–213Google Scholar
  7. 7.
    Mankel A, Krause K, Kothe E (2002) Identification of a hydrophobin gene that is developmentally regulated in the Ectomycorrhizal fungus Tricholoma terreum. Appl Environ Microb 68:1408–1413Google Scholar
  8. 8.
    Kallio JM, Rouvinen J (2011) Amphiphilic nanotubes in the crystal structure of a biosurfactant protein hydrophobin HFBII. Chem Commun 47:9843–9845Google Scholar
  9. 9.
    Carrion S-J, Leal SM Jr, Ghannoum MA, Aimanianda V, Latge J-P, Pearlman E (2013) The RodA Hydrophobin on Aspergillus masks Dectin-1- and Dectin-2-dependent responses and enhances fungal survival in vivo. J Immunol 191:2581–2588Google Scholar
  10. 10.
    Wösten HAB (2001) Hydrophobins: multipurpose proteins. Annu Rev Microbiol 55:625–646Google Scholar
  11. 11.
    Linder MB (2009) Hydrophobins: proteins that self assemble at interfaces. Curr Opin Colloid Interface Sci 14:356–363Google Scholar
  12. 12.
    Wösten HAB, Wessels JGH (1997) Hydrophobins, from molecular structure to multiple functions in fungal development. Mycoscience 38:363–374Google Scholar
  13. 13.
    Nakari-Setälä T, Aro N, Ilmén M, Muñoz G, Kalkinnen N, Penttilä M (1997) Differential expression of the vegetative and spore bound hydrophobins of Trichoderma reesei cloning and characterization of hfb2 gene. Eur J Biochem 248:415–423Google Scholar
  14. 14.
    Sunde M, Kwan AHY, Templeton MD, Beever RE, Mackay JP (2008) Structural analysis of hydrophobins. Micron 39:773–784Google Scholar
  15. 15.
    Hektor HJ, Scholtmeijer K (2005) Hydrophobins: proteins with potential. Curr Opin Biotech 16:434–439Google Scholar
  16. 16.
    Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME (2005) Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev 29:877–896Google Scholar
  17. 17.
    Kisko K, Szilvay GR, Vainio U, Linder MB, Serimaa R (2008) Interactions of hydrophobin proteins in solution studied by small-angle X-ray scattering. Biophys J 94:198–206Google Scholar
  18. 18.
    Askolin S, Linder M, Scholtmeijer K, Tenkanen M, Penttilä M, de Vocht ML, Wösten HAB (2006) Interaction and comparison of a Class I hydrophobin from Schizophyllum commune and Class II hydrophobins from Trichoderma reesei. Biomacromolecules 7:1295–1301Google Scholar
  19. 19.
    Grünbacher A, Throm T, Seidel C, Gutt B, Röhrig J, Strunk T, Vincze P, Walheim S, Schimmel T, Wenzel W, Fischer R (2014) Six hydrophobins are involved in hydrophobin rodlet formation in Aspergillus nidulans and contribute to hydrophobicity of the spore surface. PLoS ONE 9:94546–94556Google Scholar
  20. 20.
    Stanimirova RD, Gurkov TD, Kralchevsky PA, Balashev KT, Stoyanov SD, Pelan EG (2013) Surface pressure and elasticity of hydrophobin HFBII layers on the air–water interface: rheology versus structure detected by AFM imaging. Langmuir 29:6053–6067Google Scholar
  21. 21.
    Wessels JGH (1994) Developmental regulation of fungal cell wall formation. Annu Rev Phytopathol 32:413–437Google Scholar
  22. 22.
    Stringer MA, Dean RA, Sewall TC, Timberlake WE (1991) Rodletless, a new Aspergillus developmental mutant induced by directed gene inactivation. Gene Dev 5:1161–1171Google Scholar
  23. 23.
    Linder M, Selber K, Nakari-Setälä T, Qiao M, Kula M-R, Penttilä M (2001) The hydrophobins HFBI and HFBII from Trichoderma reesei showing efficient interactions with nonionic surfactants in aqueous two-phase systems. Biomacromolecules 2:511–517Google Scholar
  24. 24.
    Khalesi M, Venken T, Deckers S, Winterburn J, Shokribousjein Z, Gebruers K, Verachtert H, Delcour J, Martin P, Derdelinckx G (2013) A novel method for hydrophobin extraction using CO2 foam fractionation system. Ind Crop Prod 43:372–377Google Scholar
  25. 25.
    Askolin S, Penttilä M, Wösten HAB, Nakari-Setälä T (2005) The Trichoderma reesei hydrophobin genes hfb1 and hfb2 have diversal functions in fungal development. FEMS Microbiol Lett 253:281–288Google Scholar
  26. 26.
    Khalesi M, Zune Q, Telek S, Riveros-Galan D, Verachtert H, Toye D, Gebruers K, Derdelinckx G, Delvigne F (2014) Fungal biofilm reactor improves the productivity of hydrophobin HFBII. Biochem Eng J 88:171–178Google Scholar
  27. 27.
    Hegde RS, Bernstein HD (2006) The surprising complexity of signal sequences. Trends Biochem Sci 31:563–571Google Scholar
  28. 28.
    Emanuelsson O, Brunak S, von Heijne G, Nielsen H (2007) Locating proteins in the cell using TargetP, SignalP, and related tools. Nat Protoc 2:953–971Google Scholar
  29. 29.
    Hakanpää J, Paananen A, Askolin S, Nakari-Setälä T, Parkkinen T, Penttilä ME, Linder MB, Rouvinen J (2004) Atomic resolution structure of the HFBII hydrophobin, a self-assembling amphiphile. J Biol Chem 279:534–539Google Scholar
  30. 30.
    Szilvay GR, Kisko K, Serimaa R, Linder MB (2007) The relation between solution association and surface activity of the hydrophobin HFBI from Trichoderma reseei. FEBS Lett 581:2721–2726Google Scholar
  31. 31.
    Cox AR, Cagnolm F, Russell AB, Izzard MJ (2007) Surface properties of class II hydrophobins from Trichoderma reesei and influence on bubble stability. Langmuir 23:7995–8002Google Scholar
  32. 32.
    Helm E, Richardt OC (1938) Das Ueberschäumen (Wildwerden) des Bieres. Wochenschrift für Brauerei 55(12):89–94Google Scholar
  33. 33.
    Gardner RJ (1973) The mechanism of gushing—a review. J Inst Brewing 79:275–283Google Scholar
  34. 34.
    Haikara A, Sarlin T, Nakari-Setälä T, Penttilä M (2000) Method for determining a gushing factor for a beverage. Patent EP 1071949Google Scholar
  35. 35.
    Sarlin T, Kivioja T, Kalkkinen N, Linder MB, Nakari-Setälä T (2012) Identification and characterization of gushing-active hydrophobins from Fusarium graminearum and related species. J Basic Microb 52:184–194Google Scholar
  36. 36.
    Buxaderas S, Lopez-Tamames E (2012) Sparkling wines: features and trends from tradition. Adv Food Nutr Res 66:1–45Google Scholar
  37. 37.
    Lutterschmid G, Stübner M, Vogel RF, Niessen L (2010) Induction of gushing with recombinant Class II hydrophobin FcHyd5p from Fusarium culmorum and the impact of hop compounds on its gushing potential. J Inst Brewing 116:339–347Google Scholar
  38. 38.
    Deckers S, Vissers L, Khalesi M, Shokribousjein Z, Verachtert H, Gebruers K, Pirlot X, Rock J, Illberg V, Titze J, Neven H, Derdelinckx G (2013) Thermodynamic view of primary gushing. J Am Soc Brew Chem 71(3):149–152Google Scholar
  39. 39.
    Sarlin T, Laitila A, Pekkarinen A, Haikara A (2005) Effects of three Fusarium species on the quality of barley and malt. J Am Soc Brew Chem 63:43–49Google Scholar
  40. 40.
    Hippeli S, Elstner EF (2002) Are hydrophobins and/or non-specific lipid transfer proteins responsible for gushing in beer? New hypotheses on the chemical nature of gushing inducing factors. Verlag der Zeitschrift für Naturforschung, Tübingen www.znaturforsch.com, 1–7
  41. 41.
    Sarlin T, Nakari-Setälä T, Linder M, Penttilä M, Haikara A (2005) Fungal hydrophobins as predictors of the gushing activity of malt. J Inst Brewing 111:105–111Google Scholar
  42. 42.
    Shokribousjein Z (2014) Interaction of class II hydrophobins with hydrophobic interfaces as a basis for solving primary gushing problems in the brewing industry. Dissertation, KU Leuven, BelgiumGoogle Scholar
  43. 43.
    Christian M, Titze T, Ilberg V, Jacob F (2010) Combined particle analysis as a new tool to predict gushing shown with alcohol-free beverage products. BrewingScience 63:72–79Google Scholar
  44. 44.
    Christian M, Titze J, Ilberg V, Jacob F (2011) Novel perspectives in gushing analysis: a review. J Inst Brewing 117:295–313Google Scholar
  45. 45.
    Shokribousjein Z, Philippaerts A, Riveros D, Titze J, Ford Y, Deckers SM, Khalesi M, Delcour JA, Gebruers K, Verachtert H, Ilberg V, Derdelinckx G, Sels B (2014) A curative method for primary gushing of beer and carbonated beverages: characterization and application of antifoam based on hop oils. J Am Soc Brew Chem 72:12–21Google Scholar
  46. 46.
    Deckers S, Venken T, Khalesi M, Gebruers K, Baggerman G, Lorgouilloux Y, Shokribousjein Z, Ilberg V, Schönberger C, Titze J, Verachtert H, Michiels C, Neven H, Delcour J, Martens J, Derdelinckx G, De Maeyer M (2012) Combined modeling and biophysical characterisation of CO2 interaction with class II hydrophobins: new insight into the mechanism underpinning primary gushing. J Am Soc Brew Chem 70:249–256Google Scholar
  47. 47.
    Deckers SM, Gebruers K, Baggerman G, Lorgouilloux Y, Delcour JA, Michiels C, Derdelinckx G, Martens J, Neven H (2010) CO2-hydrophobin structures acting as nanobombs in beer. BrewingScience 63:54–61Google Scholar
  48. 48.
    Deckers SM, Lorgouilloux Y, Gebruers K, Baggerman G, Verachtert H, Neven H, Michiels C, Derdelinckx G, Delcour JA, Martens J (2011) Dynamic light scattering (DLS) as a tool to detect CO2-hydrophobin structures and study the primary gushing potential of beer. J Am Soc Brew Chem 69:144–149Google Scholar
  49. 49.
    Khalesi M, Mandelings N, Herrera-Malaver B, Riverso-Galan D, Gebruers K, Derdelinckx G (2015) Improvement of the retention of ocimene in water phase using Class II hydrophobin HFBII. Flavour Frag J. doi: 10.1002/ffj.3260 Google Scholar
  50. 50.
    Bailey MJ, Askolin S, Hörhammer N, Tenkanen M, Linder M, Penttilä M, Nakari-Setälä T (2002) Process technological effects of deletion and amplification of hydrophobins I and II in transformants of Trichoderma reesei. Appl Microbiol Biot 58:721–727Google Scholar
  51. 51.
    Askolin S, Nakari-Setälä T, Tenkanen M (2001) Overproduction, purification and characterization of the Trichoderma reesei hydrophobin HFBI. Appl Microbiol Biot 57:124–130Google Scholar
  52. 52.
    Lumsdon SO, Green J, Stieglitz B (2005) Adsorption of hydrophobin proteins at hydrophobic and hydrophilic interfaces. Colloid Surf B 44(4):172–178Google Scholar
  53. 53.
    Cox AR, Aldred DL, Russell AB (2009) Exceptional stability of food foams using class II hydrophobin HFBII. Food Hydrocolloid 23:366–376Google Scholar
  54. 54.
    Blijdenstein TBJ, de Groot PWN, Stoyanov SD (2010) On the link between foam coarsening and surface rheology: why hydrophobins are so different. Soft Matter 6:1799–1808Google Scholar
  55. 55.
    Kirkland BH, Keyhani NO (2011) Expression and purification of a functionally active class I fungal hydrophobin from the entomopathogenic fungus Beauveria bassiana in E. coli. J Ind Microbial Biot 38:327–335Google Scholar
  56. 56.
    Winterburn JB, Russell AB, Martin PJ (2011) Integrated recirculating foam fractionation for the continuous recovery of biosurfactant from fermenters. Biochem Eng J 54:132–139Google Scholar
  57. 57.
    Zune Q, Soyeurt D, Toye D, Ongena M, Thonart P, Delvigne F (2014) High-energy X-ray tomography analysis of a metal packing biofilm reactor for the production of lipopeptides by Bacillus subtilis. J Chem Technol Biotechnol 89:382–390Google Scholar
  58. 58.
    Aksay S, Mazza G (2007) Optimization of protein recovery by foam separation using response surface methodology. J Food Eng 79:598–606Google Scholar
  59. 59.
    Maruyama H, Seki H, Suzuki A, Inoue N (2007) Batch foam separation of a soluble protein. Water Res 41:710–718Google Scholar
  60. 60.
    Mukherjee S, Das P, Sen R (2006) Towards commercial production of microbial surfactants. Trends Biotechnol 24:509–515Google Scholar
  61. 61.
    Tseng H, Pilon L, Gopinath R, Warrier GR (2006) Rheology and convective heat transfer of colloidal gas aphrons in horizontal mini-channels. Int J Heat Fluid Fl 27:298–310Google Scholar
  62. 62.
    Lambert WD, Du L, Ma Y, Loha V, Burapatana V, Prokop A, Tanner RD, Pamment NB (2003) The effect of pH on the foam fractionation of β-glucosidase and cellulose. Bioresource Technol 87:247–253Google Scholar
  63. 63.
    Kallio JM, Linder MB, Rouvinen J (2007) Crystal structures of hydrophobin HFBII in the presence of detergent implicate the formation of fibrils and monolayer films. J Biol Chem 282:28733–28739Google Scholar
  64. 64.
    Szilvay GR, Paananen A, Laurikainen K, Vuorimaa E, Lemmetyinen H, Peltonen J, Linder MB (2007) Self-assembled hydrophobin protein films at the air–water interface: structural analysis and molecular engineering. Biochemistry 46:2345–2354Google Scholar
  65. 65.
    Joensuu JJ, Conley AJ, Lienemann M, Brandle JE, Linder MB, Menassa R (2010) Hydrophobin fusions for high-level transient protein expression and purification in Nicotiana benthamiana. Plant Physiol 152:622–633Google Scholar
  66. 66.
    Sarparanta MP, Bimbo LM, Mäkilä EM, Salonen JJ, Laaksonen PH, Helariutta AMK, Linder MB, Hirvonen JT, Laaksonen TJ, Santos HA, Airaksinen AJ (2012) The mucoadhesive and gastroretentive properties of hydrophobin-coated porous silicon nanoparticle oral drug delivery systems. Biomaterials 33:3353–3362Google Scholar
  67. 67.
    Vailaya A, Horvath C (1998) Retention in reversed-phase chromatography: partition or adsorption? J Chromatogr A 829:1–27Google Scholar
  68. 68.
    Janssen MI, van Leeuwen MBM, Scholtmeijer K, van Kooten TG, Dijkhuizen L, Wösten HAB (2002) Coating with genetic engineered hydrophobin promotes growth of fibroblasts on a hydrophobic solid. Biomaterials 23:4847–4854Google Scholar
  69. 69.
    Wösten HAB, Schuren FHJ, Wessels JGH (1994) Interfacial self-assembly of a hydrophobin into an amphipathic protein membrane mediates fungal attachment to hydrophobic surfaces. EMBO J 13:5848–5854Google Scholar
  70. 70.
    Qin M, Wang L-K, Feng X-Z (2007) Bioactive surface modification of mica and poly(dimethylsiloxane) with hydrophobins for protein immobilization. Langmuir 23:4465–4471Google Scholar
  71. 71.
    Mackay JP, Jacqueline K, Matthews M, Winefield RD, Mackay LG, Haverkamp RG, Templeton MD (2001) The hydrophobin EAS is largely unstructured in solution and functions by forming amyloid-like structures. Structure 9:83–91Google Scholar
  72. 72.
    Scholtmeijer K, Wessels JGH, Wösten HAB (2001) Fungal hydrophobins in medical and technical applications. Appl Microbiol Biot 56:1–8Google Scholar
  73. 73.
    Wang X, Permentier HP, Rink R, Kruijtzer JAW, Liskamp RMJ, Wösten HAB, Poolman B, Robillard GT (2004) Probing the self-assembly and the accompanying structural changes of hydrophobin SC3 on a hydrophobic surface by mass spectrometry. Biophysical J 87:1919–1928Google Scholar
  74. 74.
    Bilewicz R, Witomski J, van Der HDA, Tagu D, Palin B, Rogalska E (2001) Modification of electrodes with self-assembled hydrophobin layers. J Phys Chem B 105:9772–9777Google Scholar
  75. 75.
    Murray BS (2007) Stabilization of bubbles and foams. Curr Opin Colloid Interface Sci 12:232–241Google Scholar
  76. 76.
    Wohlleben W, Subkowski T, Bollschweiler C, von Vacano B, Liu Y, Schrepp W, Baus U (2010) Recombinantly produced hydrophobins from fungal analogues as highly surface-active performance proteins. Euro Biophys J 39:457–468Google Scholar
  77. 77.
    Tchuenbou-Magaia FL, Norton IT, Cox PW (2009) Hydrophobins stabilised air-filled emulsions for the food industry. Food Hydrocolloid 23:1877–1885Google Scholar
  78. 78.
    Valo HK, Laaksonen PH, Peltonen LJ, Linder MB, Hirvonen JT, Laaksonen TJ (2010) Multifunctional hydrophobin: toward functional coatings for drug nanoparticles. ACS Nano 4:1750–1758Google Scholar
  79. 79.
    Scholtmeijer K, Janssen MI, Gerssen B, de Vocht ML, van Leeuwen BMM, van Kooten TG, Wösten HAB, Wessels JGH (2002) Surface modifications created by using engineered hydrophobins. Appl Environ Microb 68:1367–1373Google Scholar
  80. 80.
    Linder MB, Qiao M, Laumen F, Selber K, Hyytia T, Nakari-Setälä T, Penttilä ME (2004) Efficient purification of recombinant proteins using hydrophobins as tags in surfactant-based two-phase systems. Biochemistry 43:11873–11882Google Scholar
  81. 81.
    Corvis Y, Walcarius A, Rink R, Mrabet NT, Rogalska E (2005) Preparing catalytic surfaces for sensing applications by immobilizing enzymes via hydrophobin layers. Anal Chem 77:1622–1630Google Scholar
  82. 82.
    Misra R, Li J, Cannon GC, Morgan SE (2006) Nanoscale reduction in surface friction of polymer surfaces modified with SC3 hydrophobin from Schizophyllum commune. Biomacromolecules 7:1463–1470Google Scholar
  83. 83.
    Qin M, Hou S, Wang L, Feng X, Wang R, Yang Y, Wang C, Yu L, Shao B, Qiao M (2007) Two methods for glass surface modification and their application in protein immobilization. Colloid Surf B 60:243–249Google Scholar
  84. 84.
    Lahtinen T, Linder MB, Nakari-Setälä T, Oker-Blom C (2008) Hydrophobin (HFBI): a potential fusion partner for one-step purification of recombinant proteins from insect cells. Protein Express Purif 59:18–24Google Scholar
  85. 85.
    Akanbi MHJ, Post E, Meter-Arkema A, Rink R, Robillard GT, Wang X, Wösten HAB, Scholtmeijer K (2010) Use of hydrophobins in formulation of water insoluble drugs for oral administration. Colloid Surf B 75:526–531Google Scholar
  86. 86.
    Wang X, Wang H, Huang Y, Zhao Z, Qin X, Wang Y, Miao Z, Chena Q, Qiao M (2010) Noncovalently functionalized multi-wall carbon nanotubes in aqueous solution using the hydrophobin HFBI and their electroanalytical application. Biosens Bioelectron 26:1104–1108Google Scholar
  87. 87.
    Rink R, Scholtmeijer K (2005) Method for coating an object with hydrophobin at low temperatures. Patent WO 2005068087 A2Google Scholar
  88. 88.
    Exner C, Baus U, Holoch J, Bollschweiler C, Subkowski T, Karos M, Lemaire H-G (2006) Hydrophobin as a coating agent for expandable or expanded thermoplastic polymer particles. Patent CA 2611254 A1Google Scholar
  89. 89.
    Rink R, Scholtmeijer K (2007) Method for coating an object with hydrophobin at low temperatures. Patent US 20070166346 A1Google Scholar
  90. 90.
    Aumaitre E, Farrer DB, Hedges ND, Williamson A-M, Wolf B (2009) Foaming agents comprising hydrophobin. Patent WO 2009118328 A1Google Scholar
  91. 91.
    Sweigard JA, Stieglitz B (2009) Thermophilic hydrophobin proteins and applications for surface modification. Patent US 7476537 B2Google Scholar
  92. 92.
    Barg H, Subkowski T, Karos M, Bollschweiler C (2011) Use of hydrophobin as a spreading agent. Patent WO 2010092088 A3Google Scholar
  93. 93.
    Laaksonen P, Linder M, Laaksonen T, Valo H, Hirvonen J (2012) Hydrophobins for dispersing active agents. Patent US 20120135081 A1Google Scholar
  94. 94.
    Kuil G, GROOT Petrus Wilhelmus N DE, Blijdenstein TBJ, Wieringa JA (2013) Aerated compositions containing egg albumen protein and hydrophobin. Patent WO 2013110508 A1Google Scholar
  95. 95.
    Guzmann M, Eck P, Baus U (2013) Use of hydrophobin as a phase stabiliser. Patent CA 2603374 CGoogle Scholar
  96. 96.
    Li F, You Z, Rishton V (2015) Hydrophobin composition and process for treating surfaces. Patent WO 2015051121 A1Google Scholar
  97. 97.
    Sarlin T, Vilpola A, Kotaviita E, Olkku J, Haikara A (2007) Fungal hydrophobins in the barley-to-beer chain. J Inst Brewing 113:147–153Google Scholar
  98. 98.
    Linder M, Szilvay GR, Nakari-Setälä T, Soderlund H, Penttilä M (2002) Surface adhesion of fusion proteins containing the hydrophobins HFBI and HFBII from Trichoderma reesei. Protein Sci 11:2257–2266Google Scholar
  99. 99.
    Ahlroos T, Hakala TJ, Linder MB, Holmberg K, Mahlberg R, Laaksonen P, Varjus S (2011) Biomimetic approach to water lubrication with biomolecular additives. Proc Inst Mech Eng J 225:1013–1022Google Scholar
  100. 100.
    Reuter LJ, Bailey MJ, Joensuu JJ, Ritala A (2014) A scale-up of hydrophobin-assisted recombinant protein production in tobacco BY-2 suspension cells. Plant Biotech J 12:402–410Google Scholar
  101. 101.
    Lee S, Røn T, Pakkanen KI, Linder M (2015) Hydrophobins as aqueous lubricant additive for a soft sliding contact. Colloids Surf B 125:264–269Google Scholar
  102. 102.
    Nakari-Setälä T, Aro N, Kalkkinen N, Alatalo E, Penttilä M (1996) Genetic and biochemical characterization of the Trichoderma reesei hydrophobin HFBI. Eur J Biochem 235:248–255Google Scholar
  103. 103.
    Asakawa H, Tahara S, Nakamichi M, Takehara K, Ikeno S, Linder MB, Haruyama T (2009) The amphiphilic protein HFBII as a genetically taggable molecular carrier for the formation of a self-organized functional protein layer on a solid surface. Langmuir 25:8841–8844Google Scholar
  104. 104.
    Hakanpää J, Szilvay GR, Kaljunen H, Maksimainen M, Linder MB, Rouvinen J (2006) Two crystal structures of Trichoderma reesei hydrophobin HFBI—the structure of a protein amphiphile with and without detergent interaction. Protein Sci 15(9):2129–2140Google Scholar
  105. 105.
    Hakanpaa J, Linder M, Popov A, Schmidt A, Rouvinen J (2006) Hydrophobin HFBII in detail: ultrahigh-resolution structure at 0.75 A°. Acta Cryst 62:356–367Google Scholar
  106. 106.
    Paananen A, Vuorimaa E, Torkkeli M, Penttilä M, Kauranen M, Ikkala Olli, Lemmetyinen H, Serimaa R, Linder MB (2003) Structural hierarchy in molecular films of two class II hydrophobins. Biochemistry 42:5253–5258Google Scholar
  107. 107.
    Milani R, Pirrie L, Gazzera L, Paananen A, Baldrighi M, Monogioudi E, Cavallo G, Linder M, Resnati G, Metrangolo P (2015) A synthetically modified hydrophobin showing enhanced fluorous affinity. J Colloid Interface Sci 448:140–147Google Scholar
  108. 108.
    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 68:3385–3391Google Scholar
  109. 109.
    Kurppaa K, Hytönen VP, Nakari-Setäläa T, Kulomaa MS, Linder MB (2014) Molecular engineering of avidin and hydrophobin for functional self-assembling interfaces. Colloids Surf B 120:102–109Google Scholar
  110. 110.
    Grunér MS, Szilvay GR, Berglin M, Lienemann M, Laaksonen P, Linder MB (2012) Self-assembly of Class II hydrophobins on polar surfaces. Langmuir 28:4293–4300Google Scholar
  111. 111.
    Sarparanta M, Bimbo LM, Rytkönen J, Mäkilä E, Laaksonen TJ, Laaksonen P, Nyman M, Salonen J, Linder MB, Hirvonen J, Santos HA, Airaksinen AJ (2012) Intravenous delivery of hydrophobin-functionalized porous silicon nanoparticles: stability, plasma protein adsorption and biodistribution. Mol Pharm 9:654–663Google Scholar
  112. 112.
    Pigliacelli C, D’Elicio A, Milani R, Terraneo G, Resnati G, Bombelli FB, Metrangolo P (2015) Hydrophobin-stabilized dispersions of PVDF nanoparticles in water. J Fluor Chem. doi: 10.1016/j.jfluchem.2015.02.004 Google Scholar
  113. 113.
    Wessels JGH (2000) Hydrophobins, unique fungal proteins. Mycologist 4:153–159Google Scholar
  114. 114.
    Zampieri F, Wösten HAB, Scholtmeijer K (2010) Creating surface properties using a palette of hydrophobins. Materials 3:4607–4625Google Scholar
  115. 115.
    Wösten HAB, Scholtmeijer K (2015) Applications of hydrophobins: current state and perspectives. Appl Microbiol Biot 99(4):1587–1597Google Scholar
  116. 116.
    Akanbi MHJ, Post E, van Putten SM, de Vries L, Smisterova J, Meter-Arkema AH, Wösten HAB, Rink R, Scholtmeijer K (2013) The antitumor activity of hydrophobin SC3, a fungal protein. Appl Microbiol Biotechnol 97:4385–4392Google Scholar
  117. 117.
    Basheva ES, Kralchevsky PA, Christov NC, Danov KD, Stoyanov SD, Blijdenstein TBJ, Kim H-J, Pelan EG, Lips A (2011) Unique properties of bubbles and foam films stabilized by HFBII hydrophobin. Langmuir 27:2382–2392Google Scholar
  118. 118.
    Radulova GM, Golemanov K, Danov KD, Kralchevsky PA, Stoyanov SD, Arnaudov LN, Blijdenstein TBJ, Pelan EG, Lips A (2012) Surface shear rheology of adsorption layers from the protein HFBII hydrophobin: effect of added β-casein. Langmuir 28:4168–4177Google Scholar
  119. 119.
    Alexandrov NA, Marinova KG, Gurkov TD, Danov KD, Kralchevsky PA, Stoyanov SD, Blijdenstein TBJ, Arnaudov LN, Pelan EG, Lips A (2012) Interfacial layers from the protein HFBII hydrophobin: dynamic surface tension, dilatational elasticity and relaxation times. J Colloid Interface Sci 376:296–306Google Scholar
  120. 120.
    Danov KD, Radulova GM, Kralchevsky PA, Golemanov K, Stoyanov SD (2012) Surface shear rheology of hydrophobin adsorption layers: laws of viscoelastic behaviour with applications to long-term foam stability. Faraday Discuss 158:195–221Google Scholar
  121. 121.
    Stanimirova RD, Marinova KG, Danov KD, Kralchevsky PA, Basheva ES, Stoyanov SD, Pelan EG (2014) Competitive adsorption of the protein hydrophobin and an ionic surfactant: parallel vs sequential adsorption and dilatational rheology. Colloid Surf A 457:307–317Google Scholar
  122. 122.
    Basheva ES, Kralchevsky PA, Danov KD, Stoyanov SD, Blijdenstein TBJ, Pelan EG, Lips A (2011) Self-assembled bilayers from the protein HFBII hydrophobin: nature of the adhesion energy. Langmuir 27:4481–4488Google Scholar
  123. 123.
    Wang Y, Bouillon C, Cox A, Dickinson E, Durga K, Murray BS, Xu R (2013) Interfacial study of class II hydrophobin and its mixtures with milk proteins: relationship to bubble stability. J Agric Food Chem 61:1554–1562Google Scholar
  124. 124.
    Burke J, Cox A, Petkov J, Murray BS (2014) Interfacial rheology and stability of air bubbles stabilized by mixtures of hydrophobin and β-casein. Food Hydrocolloid 34:119–127Google Scholar
  125. 125.
    Tucker IM, Petkov JT, Penfold J, Thomas RK, Li P, Cox AR, Hedges N, Webster JRP (2014) Spontaneous surface self-assembly in protein-surfactant mixtures: interactions between hydrophobin and ethoxylated polysorbate surfactants. J Phys Chem B 118:4867–4875Google Scholar
  126. 126.
    Zhang XL, Penfold J, Thomas RK, Tucker IM, Petkov JT, Bent J, Cox A (2011) Adsorption behavior of hydrophobin and hydrophobin/surfactant mixtures at the solid-solution interface. Langmuir 27:10464–10474Google Scholar
  127. 127.
    Zhang XL, Penfold J, Thomas RK, Tucker IM, Petkov JT, Bent J, Cox A, Grillo I (2011) Self-assembly of hydrophobin and hydrophobin/surfactant mixtures in aqueous solution. Langmuir 27:10514–10522Google Scholar
  128. 128.
    Zhang XL, Penfold J, Thomas RK, Tucker IM, Petkov JT, Bent J, Cox A, Campbell RA (2011) Adsorption behavior of hydrophobin and hydrophobin/surfactant mixtures at the air–water interface. Langmuir 27:11316–11323Google Scholar
  129. 129.
    Aldred DL, Berry MJ, Cebula DJ, Cox AR, Golding MD, Golding S, Keenan RD, Malone ME, Twigg S (2006) Aerated food products containing hydrophobin. Patent WO 2006010426 A1Google Scholar
  130. 130.
    Cox AR (2013) Foaming agents comprising hydrophobin. Patent US 20130216655 A1Google Scholar
  131. 131.
    Cox AR, Russell AB, Watts KM (2014) Aerated compositions comprising hydrophobin. Patent CA 2617548 CGoogle Scholar
  132. 132.
    Cox AR, Hedges ND, Rossetti D, Kristensen JB (2014) Stabilized aerated frozen confection containing hydrophobin. Patent WO 2014026885 A1Google Scholar
  133. 133.
    Deckers S, Derdelinckx G, Khalesi M, Riveros-Galan DS, Shokribousjein Z, Verachtert H (2014) Bottles with means to prevent gushing. Patent WO 2014047697 A1Google Scholar
  134. 134.
    De Stefano L, Rea I, Giardina P, Armenante A, Rendina I (2008) Protein-modified porous silicon nanostructures. Adv Mater 20:1529–1533Google Scholar
  135. 135.
    Rea I, Giardina P, Longobardi S, Porro F, Casuscelli V, Rendina I, De Stefano L (2012) Hydrophobin Vmh2-glucose complexes self-assemble in nanometric biofilms. J R Soc Interface 9:2450–2456Google Scholar
  136. 136.
    Longobardi S, Gravagnuolo AM, Rea I, De Stefano L, Marino G, Giardina P (2014) Hydrophobin-coated plates as matrix-assisted laser desorption/ionization sample support for peptide/protein analysis. Anal Biochem 449:9–16Google Scholar
  137. 137.
    Longobardi S, Gravagnuolo AM, Funari R, Ventura BD, Pane F, Galano E, Amoresano A, Marino G, Giardina P (2015) A simple MALDI plate functionalization by Vmh2 hydrophobin for serial multi-enzymatic protein digestions. Anal Bioanal Chem 407:487–496Google Scholar
  138. 138.
    Frascella A, Bettini PP, Kolarik M, Comparini C, Pazzagli L, Luti S, Scala F, Scala A (2014) Interspecific variability of class II hydrophobin GEO1 in the genus Geosmithia. Fungal Biol 118:862–871Google Scholar
  139. 139.
    Carresi L, Comparini C, Bettini PP, Pazzagli L, Cappugi G, Scala F, Scala A (2008) Isolation of the orthologue of the cerato-ulmin gene in Ophiostoma quercus and characterization of the purified protein. Mycol Res 112:1245–1255Google Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Mohammadreza Khalesi
    • 1
    • 2
    Email author
  • Kurt Gebruers
    • 1
  • Guy Derdelinckx
    • 1
  1. 1.Department of Microbial and Molecular Systems (M2S)KU LeuvenHeverleeBelgium
  2. 2.Institute of Biochemistry and BiophysicsUniversity of TehranTehranIran

Personalised recommendations