Fungal hydrophobins

This section is a summary of the review "Hydrophobins: multipurpose proteins" by H.A.B. Wösten, Annu Rev Microbiol. 2001;55:625-46.

 Filamentous fungi colonise living or dead moist substrates by means of hyphae that extend at their apices, while branching subapically. After a submerged feeding mycelium has been established, aerial hyphae are formed that may develop into reproductive structures such as conidiophores or fruiting bodies (e.g. mushrooms or brackets). Spores that are formed by these structures are dispersed and may give rise to new colonising mycelia. In these and other stages in the life cycle of filamentous fungi small secreted proteins, called hydrophobins, fulfil a broad spectrum of functions (1,2).  

Hydrophobins are proteins that occur uniquely in mycelial fungi. These proteins and their encoding genes have been isolated from ascomycetes and basidiomycetes (1). Some evidence indicates that hydrophobins occur in zygomycetes as well (3) but it is not yet clear whether they occur in the chytridiomycetes. Based on their hydropathy patterns and their solubility characteristics, class I and class II hydrophobins were distinguished (4). Class I hydrophobins have been identified in both ascomycetes and basidiomycetes but until now class II hydrophobins have been found in ascomycetes only.

Hydrophobins allow fungi to escape their aqueous environment (2), confer hydrophobicity to fungal surfaces in contact with air (5-12) and mediate attachment of hyphae to hydrophobic surfaces (13,14) resulting in morphogenetic signals (15). The latter is important in initial steps of fungal pathogenesis where the fungus must attach to the hydrophobic surface of the host before penetration and infection can occur. Moreover, hydrophobins seem to function in cases of symbioses between fungi and plants (ectomycorrhizae) (16) or algae and/or cyanobacteria (lichens) (17, 18). The mechanism underlying all these functions is based on the property of hydrophobins to self-assemble at a hydrophilic/hydrophobic interface into an amphipathic membrane (19-22). Upon self-assembly at the interface  between the hydrophilic cell wall and a hydrophobic environment (the air or the hydrophobic surface of a host), the hydrophilic side of the amphipathic membrane will orient and attach itself to the cell wall, while the hydrophobic side becomes exposed to the hydrophobic environment. Aerial hyphae and spores thus become hydrophobic, while hyphae that grow over a hydrophobic substrate attach themselves.

Recently, it was shown that hydrophobins not only function at hydrophilic-hydrophobic interfaces but also function within the matrix of the cell wall where they influence cell wall composition (23). The mechanism is not yet clear. Moreover, the class II hydrophobin cerato-ulmin is a toxin for elm that seems to function as a monomer by increasing the permeability of the plant plasma membrane (24).   
 

  1. Wessels JGH. 1997. Hydrophobins, proteins that change the nature of the fungal surface. Adv. Microbial Physiol. 38:1-45
  2. Wösten HAB, van Wetter M-A, Lugones LG, van der Mei HC, Busscher HJ, Wessels JGH. 1999. How a fungus escapes the water to grow into the air. Curr. Biol. 9:85-8
  3. de Vries OMH, Fekkes MP, Wösten HAB, Wessels JGH. 1993. Insoluble hydrophobin complexes in the walls of Schizophyllum commune and other filamentous fungi. Arch. Microbiol. 159:330-5
  4. Wessels JGH. 1994. Developmental regulation of fungal cell wall formation. Ann. Rev. Phytopathol. 32:413-3
  5. Bell-Pedersen D, Dunlap JC, Loros JJ. 1992. The Neurospora circadian clock-controlled gene, ccg-2, is allelic to eas and encodes a fungal hydrophobin required for formation of the conidial rodlet layer.  Genes Dev. 6:2382-94 
  6. Lauter FR, Russo VE, Yanofsky C. 1992. Developmental and light regulation ofeas, the structural gene for the rodlet protein of Neurospora. Genes Dev. 6:2373-81 
  7. Lugones LG, Bosscher JS, Scholtmeijer K, de Vries OMH, Wessels JGH. 1996. An abundant hydrophobin (ABH1) forms hydrophobic rodlet layers in Agaricus bisporus fruiting bodies. Microbiology 142:1321-9
  8. Lugones LG, Wösten HAB, Birkenkamp KU, Sjollema KA, Zagers J, Wessels JGH. 1999. Hydrophobins line air channels in fruiting bodies of Schizophyllum commune and Agaricus bisporus. Mycol. Res. 103:635-40
  9. Stringer MA, Dean RA, Sewall TC, Timberlake WE. 1991. Rodletless, a newAspergillus developmental mutant induced by directed gene inactivation. Genes Dev. 5:1161-71 
  10. Talbot NJ, Kershaw M, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE. 1996.MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of the rice blast fungus Magnaporthe grisea. Plant Cell 8:985-99
  11. Thau N, Monod M, Crestani B, Rolland C, Tronchin G, Latge JP, Paris S. 1994. Rodletless mutants of Aspergillus fumigatus. Infection Immun. 62:4380-8
  12. van Wetter M-A, Wösten HAB, Wessels JGH. 2000. SC3 and SC4 hydrophobins have distinct functions in formation of aerial structures in dikaryons ofSchizophyllum commune. Mol. Microbiol. 36:201-10
  13. Temple B, Horgen PA, Bernier L, Hintz WE. 1997. Cerato-ulmin, a hydrophobin secreted by the causal agents of Dutch elm disease, is a parasitic fitness factor. Fungal Genet. Biol. 22:39-53 
  14. 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. 13:5848-54 
  15. Talbot NJ, Kershaw M, Wakley GE, de Vries OMH, Wessels JGH, Hamer JE. 1996.MPG1 encodes a fungal hydrophobin involved in surface interactions during infection-related development of the rice blast fungus Magnaporthe grisea. Plant Cell 8:985-99 
  16. Tagu D, Nasse B, Martin F. 1996. Cloning and and characterization of hydrophobin-encoding cDNAs from the ectomycorrhizal basidiomycete Pisolithus tinctorius. Gene 168:93-7 
  17. Honegger R. 1991. Functional aspects of the lichen symbiosis. Ann. Rev. Plant Physiol. Plant Mol. Biol. 42:553-78 
  18. Scherrer S, de Vries OMH, Dudler R, Wessels JGH, Honegger R. 2000. Interfacial self-assembly of fungal hydrophobins of the lichen-forming ascomycetesXanthoria parietina and X. etaneoides. Fungal Genet. Biol. 30:81-93 
  19. Wösten HAB, Ásgeirsdóttir SA, Krook JH, Drenth JHH, Wessels JGH. 1994. The Sc3p hydrophobin self-assembles at the surface of aerial hyphae as a protein membrane constituting the hydrophobic rodlet layer. Eur. J. Cell Biol. 63:122-9
  20. Wösten HAB, de Vries OMH, Wessels JGH. 1993. Interfacial self-assembly of a fungal hydrophobin into a rodlet layer. Plant Cell 5:1567-74
  21. Wösten HAB, Ruardy TG, van der Mei HC, Busscher HJ, Wessels JGH. 1995. Interfacial self-assembly of a Schizophyllum commune hydrophobin into an insoluble amphipathic membrane depends on surface hydrophobicity. Coll. Surf. B:Biointerf. 5:189-95
  22. 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. 13:5848-54
  23. van Wetter MA, Wösten HAB, Sietsma JH, Wessels JGH. 2001. Hydrophobin gene expression affects hyphal wall composition in Schizophyllum commune. Fungal Genet Biol. 2000; 31(2):99-104.
  24. Stevenson KJ, Slater JA, Takai S. 1979. Cerato-ulmin, a wilting toxin of Dutch elm disease fungus. Phytochemistry 18:235-8