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Hydrophobins: the Amphiphilic Proteins Produced in Filamentous Fungi

Year 2023, Volume: 2 Issue: 1, 35 - 41, 18.04.2023

Büşra Albayrak Turgut Serkan Örtucu

Abstract

Hydrophobins are proteins of small molecular mass produced by fungi. They are part of various tasks at different stages of the life cycle of fungi, especially produced during the formation of aerial structures. They are very stable in their amphiphilic structure and thanks to the four disulfide bonds they contain. They can form a monolayer by self-assembly at the water-air, air-solid interfaces and are therefore important candidates for many industrial applications. For example; in surface modifications, they can make hydrophilic surfaces hydrophobic and hydrophobic ones hydrophilic. In addition, due to their high hydrophobicity, they prevent microorganisms from adhering to the surface or enable the fungi species from which they are produced to adhere to hydrophobic surfaces. This review article will analyze the detailed investigation of hydrophobins and the applications they have been tried and recommended for use.

Keywords

Hydrophobins Surfactant amphiphilic proteins surface modification

References

  • 1. Linder MB. Hydrophobins: Proteins That Self Assemble at Interfaces. Current Opinion in Colloid & Interface Science 2009:14 (5);356–363.
  • 2. Sarlin T, Kivioja T, Kalkkinen N, Linder MB, Nakari-Setälä T. Identification and Characterization of Gushing-Active Hydrophobins from Fusarium Graminearum and Related Species. J. Basic Microbiol. 2012:52(2);184–194.
  • 3. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME. Hydrophobins: The Protein-Amphiphiles of Filamentous Fungi. FEMS Microbiol Rev 2005:29(5);877–896.
  • 4. Wösten HAB. Hydrophobins: Multipurpose Proteins. Annu. Rev. Microbiol 2001:55 (1);625–646.
  • 5. de Vries OMH, Moore S, Arntz C, Wessels JGH; Tudzynski P. Identification and Characterization of a Tri-Partite Hydrophobin from Claviceps fusiformis. A Novel Type of Class II Hydrophobin. Eur J Biochem 1999:262 (2);377–385.
  • 6. Sunde M, Kwan AHY, Templeton MD, Beever RE, Mackay JP. Structural Analysis of Hydrophobins. Micron 2008:39(7);773–784.
  • 7. Carrion SJ, Leal SM, Ghannoum MA, Aimanianda V, Latgé JP, Pearlman E. The RodA Hydrophobin on Aspergillus Fumigatus Spores Masks Dectin-1– and Dectin-2–Dependent Responses and Enhances Fungal Survival In Vivo. The Journal of Immunology 2013:191(5);2581–2588.
  • 8. Wang Z, Lienemann M, Qiau M, Linder MB. Mechanisms of Protein Adhesion on Surface Films of Hydrophobin. Langmuir 2010:26 (11);8491–8496.
  • 9. Gómez-Pérez D, Chaudhry V, Kemen A, Kemen E. Amyloid Proteins in Plant-Associated Microbial Communities. Microbial Physiology 2021:31(2);88-98.
  • 10. Talbot NJ, Kershaw MJ, Wakley GE, deVries OMH, Wessels JGH, Hamer JE. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 1996:8(6);985-999.
  • 11. Zhang S, Xia YX, Kim B, Keyhani NO. Two Hydrophobins Are Involved in Fungal Spore Coat Rodlet Layer Assembly and Each Play Distinct Roles in Surface Interactions, Development and Pathogenesis in the Entomopathogenic Fungus, Beauveria bassiana: B. Bassiana Spore Coat Hydrophobins. Molecular Microbiology 2011:80(3);811–826.
  • 12. Wessels JGH, Ásgiersdóttir SA, Birkenkamp KU, Vries OMH, Lugones LG, Scheer JMJ, et al. Genetic Regulation of Emergent Growth in Schizophyllum Commune. Can J Bot 1995:73(S1);273–281.
  • 13. Wösten HAB, van Wetter MA, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH. How a Fungus Escapes the Water to Grow into the Air. Current Biology 1999:9(2);85–88.
  • 14. Kulkarni S, Nene S, Joshi K. Production of Hydrophobins from Fungi. Process Biochemistry 2017:61;1–11.
  • 15. Kubicek CP, Baker SE, Gamauf C, Kenerley CM, Druzhinina IS. Purifying Selection and Birth-and-Death Evolution in the Class II Hydrophobin Gene Families of the Ascomycete Trichoderma/Hypocrea. BMC Evol Biol 2008:8(1); 4.
  • 16. Littlejohn KA, Hooley P, Cox PW. Bioinformatics Predicts Diverse Aspergillus Hydrophobins with Novel Properties. Food Hydrocolloids 2012:27 (2);503–516.
  • 17. Akanbi HJM. Post E, Meter-Arkema A, Rink R, Robillard GT, Wang X, et al. Use of Hydrophobins in Formulation of Water Insoluble Drugs for Oral Administration. Colloids and Surfaces. Biointerfaces 2010:75(2);526–531.
  • 18. Lunkenbein S, Takenberg M, Nimtz M, Berger RG. Characterization of a Hydrophobin of the Ascomycete Paecilomyces Farinosus. J Basic Microbiol 2011:51(4);404–414.
  • 19. Kirkland BH, Keyhani NO. Expression and Purification of a Functionally Active Class I Fungal Hydrophobin from the Entomopathogenic Fungus Beauveria bassiana in E. Coli. J Ind Microbiol Biotechnol 2011:38(2);327–335.
  • 20. Qin M, Wang LK, Feng XZ, Yang YL, Wang R, Wang C, Yu, et al. Bioactive Surface Modification of Mica and Poly(Dimethylsiloxane) with Hydrophobins for Protein Immobilization. Langmuir 2007:23(8);4465–4471.
  • 21. Hektor HJ, Scholtmeijer K. Hydrophobins: Proteins with Potential. Current Opinion in Biotechnology 2005:16(4);434–439.
  • 22. Wösten HAB, de Vocht ML. Hydrophobins, the Fungal Coat Unravelled. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes 2000:1469(2);79–86.
  • 23. Paris S, Debeaupuis JP, Crameri R, Carey M, Charlès F, Prévost MC, Schmitt, C., Philippe, B., Latgé, J.P., Conidial Hydrophobins of Aspergillus fumigatus. Appl Environ Microbiol 2003:69;1581–1588.
  • 24. Winterburn JB, Russell AB, Martin PJ. Characterisation of HFBII Biosurfactant Production and Foam Fractionation with and without Antifoaming Agents. Appl Microbiol Biotechnol 2011:90(3);911–920.
  • 25. Scholtmeijer K, Wessels JGH, Wösten HAB. Fungal Hydrophobins in Medical and Technical Applications. Applied Microbiology and Biotechnology 2001:56(1–2);1–8.
  • 26. Rabe M, Verdes D, Seeger S. Understanding Protein Adsorption Phenomena at Solid Surfaces. Advances in Colloid and Interface Science 2011:162(1–2);87–106.
  • 27. Stanzione I, Pitocchi R, Pennacchio A, Cicatiello P, Piscitelli A, Giardina P. Innovative surface bio-functionalization by fungal hydrophobins and their engineered variants. Frontiers in Molecular Biosciences 2022:9;959166.
  • 28. Rieder A, Ladnorg T, Wöll C, Obst U, Fischer R, Schwartz T. The Impact of Recombinant Fusion-Hydrophobin Coated Surfaces on E. Coli and Natural Mixed Culture Biofilm Formation. Biofouling 2011:27(10);1073–1085.
  • 29. Janssen MI, Leeuwen MBM, van Kooten TG, Vries J, Dijkhuizen L, Wösten HAB. Promotion of Fibroblast Activity by Coating with Hydrophobins in the β-Sheet End State. Biomaterials 2004:25(14);2731–2739.
  • 30. Bimbo LM, Mäkilä E, Raula J, Laaksonen T, Laaksonen P, Strommer K et al. Functional Hydrophobin-Coating of Thermally Hydrocarbonized Porous Silicon Microparticles. Biomaterials 2011:32(34);9089–9099.
  • 31. Janssen MI, van Leeuwen MBM, Scholtmeijer K, van Kooten TG, Dijkhuizen L, Wösten HAB. Coating with Genetic Engineered Hydrophobin Promotes Growth of Fibroblasts on a Hydrophobic Solid. Biomaterials 2002:23(24);4847–4854.
  • 32. Kisko K, Szilvay GR, Vainio U, Linder MB, Serimaa R. Interactions of Hydrophobin Proteins in Solution Studied by Small-Angle X-Ray Scattering. Biophysical Journal 2008:94(1);198–206.
  • 33. Khalesi M, Gebruers K, Derdelinckx G. Recent Advances in Fungal Hydrophobin Towards Using in Industry. Protein J 2015: 34(4);243–255.
  • 34. Chakarova SD, Carlsson AE. Model Study of Protein Unfolding by Interfaces. Phys Rev E 2004, 69 (2), 021907.
  • 35. Neinhuis C. Characterization and Distribution of Water-Repellent, Self-Cleaning Plant Surfaces. Annals of Botany 1997:79(6);667–677.
  • 36. Wagner P, Fürstner R, Barthlott W, Neinhuis C. Quantitative Assessment to the Structural Basis of Water Repellency in Natural and Technical Surfaces. Journal of Experimental Botany 2003:54(385);1295–1303.
  • 37. Starov VM, Velarde MG, Radke CJ. Wetting and spreading Dynamics. 1st ed. Boca Raton, Florida:CRC press;2007.
  • 38. Wösten, H. A. B.; Scholtmeijer, K. Applications of Hydrophobins: Current State and Perspectives. Appl Microbiol Biotechnol 2015: 99(4);1587–1597.
  • 39. Vergara-Fernández A, Van Haaren B, Revah S. Phase Partition of Gaseous Hexane and Surface Hydrophobicity of Fusarium Solani When Grown in Liquid and Solid Media with Hexanol and Hexane. Biotechnol Lett 2006:28(24);2011–2017.
  • 40. Bayry J, Aimanianda V, Guijarro JI, Sunde M, Latgé JP. Hydrophobins—Unique Fungal Proteins. PLoS Pathogy 2012:8 (5);e1002700.
  • 41. Scholtmeijer K, Wessels JGH, Wösten HAB. Fungal Hydrophobins in Medical and Technical Applications. Applied Microbiology and Biotechnology 2001:56(1–2);1–8.
  • 42. Khalesi M, Venken T, Deckers S, Winterburn J, Shokribousjein Z, Gebruers K. A Novel Method for Hydrophobin Extraction Using CO2 Foam Fractionation System. Industrial Crops and Products 2013:43;372–377.
  • 43. Khalesi M, Zune Q, Telek S, Riveros-Galan D, Verachtert H, Toye D. Fungal Biofilm Reactor Improves the Productivity of Hydrophobin HFBII. Biochemical Engineering Journal 2014:88;171–178.
  • 44. Takai S. Cerato-Ulmin, a Wilting Toxin of Ceratocystis Ulmi: Cultural Factors Affecting Cerato-Ulmin Production by the Fungus. J Phytopathol 1978:91(2);147–158.
  • 45. Pedersen MH, Borodina I, Moresco JL, Svendsen WE, Frisvad JC, Søndergaard I. High-Yield Production of Hydrophobins RodA and RodB from Aspergillus Fumigatus in Pichia pastoris. Appl Microbiol Biotechnol 2011:90(6);1923–1932.
  • 46. Vigueras G, Arriaga S, Shirai K, Morales M, Revah S. Hydrophobic Response of the Fungus Rhinocladiella Similis in the Biofiltration with Volatile Organic Compounds with Different Polarity. Biotechnol Lett 2009:31(8);1203–1209.
  • 47. Yin, SH, Feng MG. Relationship between Thermotolerance and Hydrophobin-like Proteins in Aerial Conidia of Beauveria bassiana and Paecilomyces Fumosoroseus as Fungal Biocontrol Agents. J Appl Microbiol 2004:97(2);323–331.
  • 48. Vigueras G, Shirai K, Martins D, Franco TT, Fleuri LF, Revah S. Toluene Gas Phase Biofiltration by Paecilomyces Lilacinus and Isolation and Identification of a Hydrophobin Protein Produced Thereof. Appl Microbiol Biotechnol 2008:80(1);147.

Year 2023, Volume: 2 Issue: 1, 35 - 41, 18.04.2023

Büşra Albayrak Turgut Serkan Örtucu

Abstract

References

  • 1. Linder MB. Hydrophobins: Proteins That Self Assemble at Interfaces. Current Opinion in Colloid & Interface Science 2009:14 (5);356–363.
  • 2. Sarlin T, Kivioja T, Kalkkinen N, Linder MB, Nakari-Setälä T. Identification and Characterization of Gushing-Active Hydrophobins from Fusarium Graminearum and Related Species. J. Basic Microbiol. 2012:52(2);184–194.
  • 3. Linder MB, Szilvay GR, Nakari-Setälä T, Penttilä ME. Hydrophobins: The Protein-Amphiphiles of Filamentous Fungi. FEMS Microbiol Rev 2005:29(5);877–896.
  • 4. Wösten HAB. Hydrophobins: Multipurpose Proteins. Annu. Rev. Microbiol 2001:55 (1);625–646.
  • 5. de Vries OMH, Moore S, Arntz C, Wessels JGH; Tudzynski P. Identification and Characterization of a Tri-Partite Hydrophobin from Claviceps fusiformis. A Novel Type of Class II Hydrophobin. Eur J Biochem 1999:262 (2);377–385.
  • 6. Sunde M, Kwan AHY, Templeton MD, Beever RE, Mackay JP. Structural Analysis of Hydrophobins. Micron 2008:39(7);773–784.
  • 7. Carrion SJ, Leal SM, Ghannoum MA, Aimanianda V, Latgé JP, Pearlman E. The RodA Hydrophobin on Aspergillus Fumigatus Spores Masks Dectin-1– and Dectin-2–Dependent Responses and Enhances Fungal Survival In Vivo. The Journal of Immunology 2013:191(5);2581–2588.
  • 8. Wang Z, Lienemann M, Qiau M, Linder MB. Mechanisms of Protein Adhesion on Surface Films of Hydrophobin. Langmuir 2010:26 (11);8491–8496.
  • 9. Gómez-Pérez D, Chaudhry V, Kemen A, Kemen E. Amyloid Proteins in Plant-Associated Microbial Communities. Microbial Physiology 2021:31(2);88-98.
  • 10. Talbot NJ, Kershaw MJ, Wakley GE, deVries OMH, Wessels JGH, Hamer JE. MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of Magnaporthe grisea. Plant Cell 1996:8(6);985-999.
  • 11. Zhang S, Xia YX, Kim B, Keyhani NO. Two Hydrophobins Are Involved in Fungal Spore Coat Rodlet Layer Assembly and Each Play Distinct Roles in Surface Interactions, Development and Pathogenesis in the Entomopathogenic Fungus, Beauveria bassiana: B. Bassiana Spore Coat Hydrophobins. Molecular Microbiology 2011:80(3);811–826.
  • 12. Wessels JGH, Ásgiersdóttir SA, Birkenkamp KU, Vries OMH, Lugones LG, Scheer JMJ, et al. Genetic Regulation of Emergent Growth in Schizophyllum Commune. Can J Bot 1995:73(S1);273–281.
  • 13. Wösten HAB, van Wetter MA, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH. How a Fungus Escapes the Water to Grow into the Air. Current Biology 1999:9(2);85–88.
  • 14. Kulkarni S, Nene S, Joshi K. Production of Hydrophobins from Fungi. Process Biochemistry 2017:61;1–11.
  • 15. Kubicek CP, Baker SE, Gamauf C, Kenerley CM, Druzhinina IS. Purifying Selection and Birth-and-Death Evolution in the Class II Hydrophobin Gene Families of the Ascomycete Trichoderma/Hypocrea. BMC Evol Biol 2008:8(1); 4.
  • 16. Littlejohn KA, Hooley P, Cox PW. Bioinformatics Predicts Diverse Aspergillus Hydrophobins with Novel Properties. Food Hydrocolloids 2012:27 (2);503–516.
  • 17. Akanbi HJM. Post E, Meter-Arkema A, Rink R, Robillard GT, Wang X, et al. Use of Hydrophobins in Formulation of Water Insoluble Drugs for Oral Administration. Colloids and Surfaces. Biointerfaces 2010:75(2);526–531.
  • 18. Lunkenbein S, Takenberg M, Nimtz M, Berger RG. Characterization of a Hydrophobin of the Ascomycete Paecilomyces Farinosus. J Basic Microbiol 2011:51(4);404–414.
  • 19. Kirkland BH, Keyhani NO. Expression and Purification of a Functionally Active Class I Fungal Hydrophobin from the Entomopathogenic Fungus Beauveria bassiana in E. Coli. J Ind Microbiol Biotechnol 2011:38(2);327–335.
  • 20. Qin M, Wang LK, Feng XZ, Yang YL, Wang R, Wang C, Yu, et al. Bioactive Surface Modification of Mica and Poly(Dimethylsiloxane) with Hydrophobins for Protein Immobilization. Langmuir 2007:23(8);4465–4471.
  • 21. Hektor HJ, Scholtmeijer K. Hydrophobins: Proteins with Potential. Current Opinion in Biotechnology 2005:16(4);434–439.
  • 22. Wösten HAB, de Vocht ML. Hydrophobins, the Fungal Coat Unravelled. Biochimica et Biophysica Acta (BBA) - Reviews on Biomembranes 2000:1469(2);79–86.
  • 23. Paris S, Debeaupuis JP, Crameri R, Carey M, Charlès F, Prévost MC, Schmitt, C., Philippe, B., Latgé, J.P., Conidial Hydrophobins of Aspergillus fumigatus. Appl Environ Microbiol 2003:69;1581–1588.
  • 24. Winterburn JB, Russell AB, Martin PJ. Characterisation of HFBII Biosurfactant Production and Foam Fractionation with and without Antifoaming Agents. Appl Microbiol Biotechnol 2011:90(3);911–920.
  • 25. Scholtmeijer K, Wessels JGH, Wösten HAB. Fungal Hydrophobins in Medical and Technical Applications. Applied Microbiology and Biotechnology 2001:56(1–2);1–8.
  • 26. Rabe M, Verdes D, Seeger S. Understanding Protein Adsorption Phenomena at Solid Surfaces. Advances in Colloid and Interface Science 2011:162(1–2);87–106.
  • 27. Stanzione I, Pitocchi R, Pennacchio A, Cicatiello P, Piscitelli A, Giardina P. Innovative surface bio-functionalization by fungal hydrophobins and their engineered variants. Frontiers in Molecular Biosciences 2022:9;959166.
  • 28. Rieder A, Ladnorg T, Wöll C, Obst U, Fischer R, Schwartz T. The Impact of Recombinant Fusion-Hydrophobin Coated Surfaces on E. Coli and Natural Mixed Culture Biofilm Formation. Biofouling 2011:27(10);1073–1085.
  • 29. Janssen MI, Leeuwen MBM, van Kooten TG, Vries J, Dijkhuizen L, Wösten HAB. Promotion of Fibroblast Activity by Coating with Hydrophobins in the β-Sheet End State. Biomaterials 2004:25(14);2731–2739.
  • 30. Bimbo LM, Mäkilä E, Raula J, Laaksonen T, Laaksonen P, Strommer K et al. Functional Hydrophobin-Coating of Thermally Hydrocarbonized Porous Silicon Microparticles. Biomaterials 2011:32(34);9089–9099.
  • 31. Janssen MI, van Leeuwen MBM, Scholtmeijer K, van Kooten TG, Dijkhuizen L, Wösten HAB. Coating with Genetic Engineered Hydrophobin Promotes Growth of Fibroblasts on a Hydrophobic Solid. Biomaterials 2002:23(24);4847–4854.
  • 32. Kisko K, Szilvay GR, Vainio U, Linder MB, Serimaa R. Interactions of Hydrophobin Proteins in Solution Studied by Small-Angle X-Ray Scattering. Biophysical Journal 2008:94(1);198–206.
  • 33. Khalesi M, Gebruers K, Derdelinckx G. Recent Advances in Fungal Hydrophobin Towards Using in Industry. Protein J 2015: 34(4);243–255.
  • 34. Chakarova SD, Carlsson AE. Model Study of Protein Unfolding by Interfaces. Phys Rev E 2004, 69 (2), 021907.
  • 35. Neinhuis C. Characterization and Distribution of Water-Repellent, Self-Cleaning Plant Surfaces. Annals of Botany 1997:79(6);667–677.
  • 36. Wagner P, Fürstner R, Barthlott W, Neinhuis C. Quantitative Assessment to the Structural Basis of Water Repellency in Natural and Technical Surfaces. Journal of Experimental Botany 2003:54(385);1295–1303.
  • 37. Starov VM, Velarde MG, Radke CJ. Wetting and spreading Dynamics. 1st ed. Boca Raton, Florida:CRC press;2007.
  • 38. Wösten, H. A. B.; Scholtmeijer, K. Applications of Hydrophobins: Current State and Perspectives. Appl Microbiol Biotechnol 2015: 99(4);1587–1597.
  • 39. Vergara-Fernández A, Van Haaren B, Revah S. Phase Partition of Gaseous Hexane and Surface Hydrophobicity of Fusarium Solani When Grown in Liquid and Solid Media with Hexanol and Hexane. Biotechnol Lett 2006:28(24);2011–2017.
  • 40. Bayry J, Aimanianda V, Guijarro JI, Sunde M, Latgé JP. Hydrophobins—Unique Fungal Proteins. PLoS Pathogy 2012:8 (5);e1002700.
  • 41. Scholtmeijer K, Wessels JGH, Wösten HAB. Fungal Hydrophobins in Medical and Technical Applications. Applied Microbiology and Biotechnology 2001:56(1–2);1–8.
  • 42. Khalesi M, Venken T, Deckers S, Winterburn J, Shokribousjein Z, Gebruers K. A Novel Method for Hydrophobin Extraction Using CO2 Foam Fractionation System. Industrial Crops and Products 2013:43;372–377.
  • 43. Khalesi M, Zune Q, Telek S, Riveros-Galan D, Verachtert H, Toye D. Fungal Biofilm Reactor Improves the Productivity of Hydrophobin HFBII. Biochemical Engineering Journal 2014:88;171–178.
  • 44. Takai S. Cerato-Ulmin, a Wilting Toxin of Ceratocystis Ulmi: Cultural Factors Affecting Cerato-Ulmin Production by the Fungus. J Phytopathol 1978:91(2);147–158.
  • 45. Pedersen MH, Borodina I, Moresco JL, Svendsen WE, Frisvad JC, Søndergaard I. High-Yield Production of Hydrophobins RodA and RodB from Aspergillus Fumigatus in Pichia pastoris. Appl Microbiol Biotechnol 2011:90(6);1923–1932.
  • 46. Vigueras G, Arriaga S, Shirai K, Morales M, Revah S. Hydrophobic Response of the Fungus Rhinocladiella Similis in the Biofiltration with Volatile Organic Compounds with Different Polarity. Biotechnol Lett 2009:31(8);1203–1209.
  • 47. Yin, SH, Feng MG. Relationship between Thermotolerance and Hydrophobin-like Proteins in Aerial Conidia of Beauveria bassiana and Paecilomyces Fumosoroseus as Fungal Biocontrol Agents. J Appl Microbiol 2004:97(2);323–331.
  • 48. Vigueras G, Shirai K, Martins D, Franco TT, Fleuri LF, Revah S. Toluene Gas Phase Biofiltration by Paecilomyces Lilacinus and Isolation and Identification of a Hydrophobin Protein Produced Thereof. Appl Microbiol Biotechnol 2008:80(1);147.
There are 48 citations in total.

Details

Primary Language English
Subjects Microbiology
Journal Section Research Articles
Authors

Büşra Albayrak Turgut

Serkan Örtucu

Early Pub Date March 30, 2023
Publication Date April 18, 2023
Published in Issue Year 2023 Volume: 2 Issue: 1

Cite

APA Albayrak Turgut, B., & Örtucu, S. (2023). Hydrophobins: the Amphiphilic Proteins Produced in Filamentous Fungi. Eurasian Journal of Molecular and Biochemical Sciences, 2(1), 35-41.
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