Browse > Article
http://dx.doi.org/10.14480/JM.2017.15.1.1

Fungal and mushroom hydrophobins: A review  

Wu, Yuanzheng (Ecology Institute, Shandong Academy of Sciences)
Li, Jishun (Ecology Institute, Shandong Academy of Sciences)
Yang, Hetong (Ecology Institute, Shandong Academy of Sciences)
Shin, Hyun-Jae (Department of Biochemical and Polymer Engineering, Chosun University)
Publication Information
Journal of Mushroom / v.15, no.1, 2017 , pp. 1-7 More about this Journal
Abstract
Hydrophobins are surface active proteins that are produced by filamentous fungi including mushrooms. Their ability to self-assemble into an amphipathic membrane at any hydrophilic-hydrophobic interface is most intriguing. These small secreted proteins comprise of eight conserved cysteine residues which form four disulfide bridges and an extraordinary hydrophobic patch. Hydrophobins play critical roles in fungal (and/or mushrooms) growth as structural components and in the interaction of fungi and mushrooms with the environment. The biophysical and biochemical properties of the isolated proteins are remarkable, such as strong adhesion, high surface activity and the formation of various self-assembled structures. With the increasing demands of hydrophobins from fungi and mushroom sources, production and purification in large scale is under challenge. Various applications, ranging from food industries, cosmetics, nanotechnology, biosensors and electrodes, to biomaterials and pharmaceuticals are emerging and a bright future is foreseen.
Keywords
Hydrophobin; Filamentous fungi; Mushroom; Self-assembly; Small proteins;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Scholtmeijer K. 2000. Expression and engineering of hydrophobin genes. Ph.D. thesis. University of Groningen.
2 Scholtmeijer K, Wessels JG, Wosten HA. 2001. Fungal hydrophobins in medical and technical applications. Appl Microbiol Biotechnol. 56:1-8.   DOI
3 Scholtmeijer K, Rink R, Hektor HJ, Wosten HA. 2005. Expression and engineering of fungal hydrophobins. Appl Mycol Biotechnol. 5:239-255.
4 Schuurs TA, Schaeffer EA, Wessels JG. 1997. Homologydependent silencing of the SC3 gene in Schizophyllum commune. Genetics 147:589-596.
5 Shokribousjein Z, Deckers SM, Gebruers K, Lorgouilloux Y, Baggerman G, Verachtert H, Delcour JA, Etienne P, Rock JM, Michiels C, Derdelinckx G. 2011. Hydrophobins, beer foaming and gushing. Cerevisia 35:85-101.   DOI
6 Stubner M, Lutterschmid G, Vogel RF, Niessen L. 2010. Heterologous expression of the hydrophobin FcHyd5p from Fusarium culmorum in Pichia pastoris and evaluation of its surface activity and contribution to gushing of carbonated beverages. Int J Food Microbiol. 141:110-115.   DOI
7 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 46:2345-2354.   DOI
8 Tchuenbou-Magaia FL, Norton IT, Cox PW. 2009. Hydrophobins stabilised airfilled emulsions for the food industry. Food Hydrocoll. 23:1877-1885.   DOI
9 Valo HK, Laaksonen PH, Peltonen LJ, Linder MB, Hirvonen JT, Laaksonen TJ. 2010. Multifunctional hydrophobin: toward functional coatings for drug nanoparticles. ACS Nano 4:1750-1758.   DOI
10 Vic G. 2003. Cosmetic use of at least one hydrophobin for treating keratin materials, and compositions used. US Patent Application 2003/0217419.
11 Wang X, Graveland-Bikker JF, de Kruif CG, Robillard GT. 2004. Oligomerization of hydrophobin SC3 in solution: from soluble state to self-assembly. Protein Sci. 13:810-821.   DOI
12 Aimanianda V, Bayry J, Bozza S, Kniemeyer O, Perruccio K, Elluru SR, Clavaud C, Paris S, Brakhage AA, Kaveri SV, Romani L, Latge JP. 2009. Surface hydrophobin prevents immune recognition of airborne fungal spores. Nature 460:1117-1121.   DOI
13 Armenante A. 2008. Pleurotus ostreatus hydrophobins: surface active proteins. Dottorato in Scienze Biotecnologiche - XXI ciclo, Indirizzo Biotecnologie Industriali, Universita di Napoli Federico II.
14 Askolin S, Linder M, Scholtmeijer K, Tenkanen M, Penttila M, de Vocht ML, Wosten HA. 2006. Interaction and comparison of a class I hydrophobin from Schizophyllum commune and class II hydrophobins from Trichoderma reesei. Biomacromolecules 7:1295-1301.   DOI
15 Askolin S, Nakari-Setala T, Tenkanen M. 2001. Overproduction, purification, and characterization of the Trichoderma reesei hydrophobin HFBI. Appl Microbiol Biotechnol. 57:124-130.   DOI
16 Chaplin MF, Kennedy JF. 1994. Carbohydrate analysis: a practical approach, 2nd ed. IRL Press, London.
17 Bayry J, Aimanianda V, Guijarro JI, Sunde M, Latge JP. 2012. Hydrophobins-unique fungal proteins. PLoS Pathog. 8:e1002700.   DOI
18 Bilewicz R, Witomski J, van Der HD, Tagu D, Palin B, Rogalska E. 2001. Modification of electrodes with self-assembled hydrophobin layers. J Phys Chem B. 105:9772-9777.   DOI
19 Bruns S, Kniemeyer O, Hasenberg M, Aimanianda V, Nietzsche S, Thywissen A, Jeron A, Latge JP, Brakhage AA, Gunzer M. 2010. Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog. 6:e1000873.   DOI
20 Wang X, Shi FX, Wosten HA, Hektor H, Poolman B, Robillard GT. 2005. The SC3 hydrophobin self-assembles into amembrane with distinct mass transfer properties. Biophys J. 88:3434-3443.   DOI
21 Wang Z, Feng S, Huang Y, Li S, Xu H, Zhang X, Bai Y, Qiao M. 2010. Expression and characterization of a Grifola frondosa hydrophobin in Pichia pastoris. Protein Expr Purif. 72:19-25.   DOI
22 Wessels JG. 1994. Developmental regulation of fungal cell-wall formation. Annu Rev Phytopathol. 32:413-437.   DOI
23 Wessels JG, de Vries OM, Asgeirsdóttir SA, Springer J. 1991. The thn mutation of Schizophyllum commune, which suppresses formation of aerial hyphae, affects expression of the Sc3 hydrophobin gene. J Gen Microbiol. 137:2439-2445.   DOI
24 Whiteford JR, Spanu P. 2002. Hydrophobins and the interactions between fungi and plants. Mol Plant Pathol. 3:391-400.   DOI
25 Wosten HA. 2001. Hydrophobins: multipurpose proteins. Annu Rev Microbiol. 55:625-646.   DOI
26 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. 282:28733-28739.   DOI
27 Wosten HA, de Vocht ML. 2000. Hydrophobins, the fungal coat unravelled. Biochim Biophys Acta 1469:79-86.   DOI
28 Yu L, Zhang B, Szilvay GR, Sun R, Janis J, Wang Z, Feng S, Xu H, Linder MB, Qiao M. 2008. Protein HGFI from the edible mushroom Grifola frondosa is a novel 8 kDa class I hydrophobin that forms rodlets in compressed monolayers. Microbiology 154:1677-1685.   DOI
29 Hou S, Yang K, Qin M, Feng XZ, Guan L, Yang Y, Wang C. 2008. Patterning of cells on functionalized poly(dimethylsiloxane) surface prepared by hydrophobin and collagen modification. Biosens Bioelectron. 24:912-916.   DOI
30 Houmadi S, Ciuchi F, De Santo MP, De Stefano L, Rea I, Giardina P, Armenante A, Lacaze E, Giocondo M. 2008. Langmuir-Blodgett film of hydrophobin protein from Pleurotus ostreatus at the air-water interface. Langmuir 24:12953-12957.   DOI
31 Khalesi M, Deckers SM, Gebruers K, Vissers L, Verachtert H, Derdelinckx G. 2012. Hydrophobins: Exceptional proteins for many applications in brewery environment and other bioindustries. Cerevisia 37:3-9.   DOI
32 Khalesi M, Gebruers K, Derdelinckx G. 2015. Recent advances in fungal hydrophobin towards using in industry. Protein J. 34:243-255.   DOI
33 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 38:129-134.   DOI
34 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 Microbiol Biotechnol. 38:327-335.   DOI
35 Kisko K. 2008. Characterization of hydrophobin proteins at interfaces and in solutions using X-rays. Academic Dissertation. University of Helsinki, Faculty of Science, Department of Physics.
36 Kottmeier K, Gunther TJ, Weber J, Kurtz S, Ostermann K, Rodel G, Bley T. 2012. Constitutive expression of hydrophobin HFB1 from Trichoderma reesei in Pichia pastoris and its prepurification by foam separation during cultivation. Eng Life Sci. 12:162-170.   DOI
37 Cox AR, Aldred DL, Russell AB. 2009. Exceptional stability of food foams using class II hydrophobin HFBII. Food Hydrocoll. 23:366-376.   DOI
38 Kwan AH, Macindoe I, Vukasin PV, Morris VK, Kass I, Gupte R, Mark AE, Templeton MD, Mackay JP, Sunde M. 2008. The Cys3-Cys4 loop of the hydrophobin EAS is not required for rodlet formation and surface activity. J Mol Biol. 382:708-720.   DOI
39 Collen A, Persson J, Linder MB, Nakari-Setala T, Penttila M, Tjerneld F, Sivars U. 2002. A novel two-step extraction method with detergent/polymer systems for primary recovery of the fusion protein endoglucanase I-hydrophobin I. Biochim Biophys Acta. 1569:139-150.   DOI
40 Cooper A, Kennedy MW. 2010. Biofoams and natural protein surfactants. Biophys Chem. 151:96-104.   DOI
41 Dagenais TR, Giles SS, Aimanianda V, Latge JP, Hull CM, Keller NP. 2010. Aspergillus fumigatus LaeA-mediated phagocytosis is associated with a decreased hydrophobin layer. Infect Immun. 78:823-829.   DOI
42 De Stefano L, Rea I, Armenante A, Giardina P, Giocondo M, Rendina I. 2007. Self-assembled biofilm of hydrophobins protects the silicon surface in the KOH wet etch process. Langmuir 23:7920-7922.   DOI
43 De Vocht ML, Reviakine I, Wosten HA, Brisson A, Wessels JG, Robillard GT. 2000. Structural and functional role of the disulfide bridges in the hydrophobin SC3. J Biol Chem. 275:28428-28432.   DOI
44 Garbe LA, Schwarz P, Ehmer A. 2009. Beer gushing. Handbook of alcoholic beverages series, beer a quality perspective. Elsevier Ltd., pp. 185-212, Chapter 6.
45 Haas Jimoh Akanbi M, Post E, Meter-Arkema A, Rink R, Robillard GT, Wang X, Wosten HA, Scholtmeijer K. 2010. Use of hydrophobins in formulation of water insoluble drugs for oral administration. Colloids Surf B Biointerfaces 75:526-531.   DOI
46 Hakanpaa J, Paananen A, Askolin S, Nakari-Setala T, Parkkinen T, Penttila M, Linder MB, Rouvinen J. 2004. Atomic resolution structure of the HFBII hydrophobin, a selfassembling amphiphile. J Biol Chem. 279:534-539.   DOI
47 Linder MB, Qiao M, Laumen F, Selber K, Hyytia T, Nakari-Setala T, Penttila ME. 2004. Efficient purification of recombinant proteins using hydrophobins as tags in surfactant-based twophase systems. Biochemistry 43:11873-11882.   DOI
48 Kwan AH, Winefield RD, Sunde M, Matthews JM, Haverkamp RG, Templeton MD, Mackay JP. 2006. Structural basis for rodlet assembly in fungal hydrophobins. Proc Natl Acad Sci USA. 103:3621-3626.   DOI
49 Li X, Hou S, Feng X, Yu Y, Ma J, Li L. 2009. Patterning of neural stem cells on poly(lactic-coglycolic acid) film modified by hydrophobin. Colloids Surf B Biointerfaces 74:370-374.   DOI
50 Linder MB. 2009. Hydrophobins: proteins that self assemble at interfaces. Curr Opin Colloid Interface Sci. 14:356-363.   DOI
51 Linder MB, Szilvay GR, Nakari-Setala T, Penttila ME. 2005. Hydrophobins: the protein-amphiphiles of filamentous fungi. FEMS Microbiol Rev. 29:877-896.   DOI
52 Linder M, Szilvay GR, Nakari-Setala T, Soderlund H, Penttila M. 2002. Surface adhesion of fusion proteins containing the hydrophobins HFBI and HFBII from Trichoderma reesei. Protein Sci. 11:2257-2266.
53 Lumsdon SO, Green J, Stieglitz B. 2005. Adsorption of hydrophobin proteins at hydrophobic and hydrophilic interfaces. Colloids Surf B-Biointerfaces 44:172-178.   DOI
54 Lutterschmid G, Muranyi M, Stubner M, Vogel RF, Niessen L. 2011. Heterologous expression of surface-active proteins from barley and filamentous fungi in Pichia pastoris and characterization of their contribution to beer gushing. Int J Food Microbiol. 147:17-25.   DOI
55 Palomo JM, Penas MM, Fernandez-Lorente G, Mateo C, Pisabarro AG, Fernandez-Lafuente R, Ramirez L, Guisan JM. 2003. Solid-phase handling of hydrophobins: immobilized hydrophobins as a new tool to study lipases. Biomacromolecules 4:204-210.   DOI
56 Hektor HJ, Scholtmeijer K. 2005. Hydrophobins: proteins with potential. Curr Opin Biotechnol. 16:434-439.   DOI
57 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 7:1463-1470.   DOI
58 Morris VK, Linser R, Wilde KL, Duff AP, Sunde M, Kwan AH. 2012. Solid-state NMR spectroscopy of functional amyloid from a fungal hydrophobin: a well-ordered ${\beta}$-sheet core amidst structural heterogeneity. Angew Chem Int Ed Engl. 51:12621-12625.   DOI
59 Murray BS, Dickinson E, Wang Y. 2009. Bubble stability in the presence of oil-inwater emulsion droplets: influence of surface shear versus dilatational rheology. Food Hydrocoll. 23:1198-1208.   DOI
60 Niu B, Wang D, Yang Y, Xu H, Qiao M. 2012. Heterologous expression and characterization of the hydrophobin HFBI in Pichia pastoris and evaluation of its contribution to the food industry. Amino Acids 43:763-771.   DOI
61 Pedersen MH, Borodina I, Moresco JL, Svendsen WE, Frisvad JC, Sondergaard I. 2011 High-yield production of hydrophobins RodA and RodB from Aspergillus fumigatus in Pichia pastoris. Appl Microbiol Biotechnol. 90:1923-1932.   DOI
62 Sarlin T, Nakari-Seta T, Linder M, Penttila M, Haikara A. 2005. Fungal hydrophobins as predictors of the gushing activity of malt. J Inst Brew. 111:105-111.   DOI
63 Schmoll M, Seibel C, Kotlowski C, Wollert Genannt Vendt F, Liebmann B, Kubicek CP. 2010. Recombinant production of an Aspergillus nidulans class I hydrophobin (DewA) in Hypocrea jecorina (Trichoderma reesei) is promoterdependent. Appl Microbiol Biotechnol. 88:95-103.   DOI