Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Fungal secretomes—nature’s toolbox for white biotechnology

Abstract

Adapting their metabolism to varying carbon and nitrogen sources, saprophytic fungi produce an arsenal of extracellular enzymes, the secretome, which allows for an efficient degradation of lignocelluloses and further biopolymers. Based on fundamental advances in electrophoretic, chromatographic, and mass spectrometric techniques on the one hand and the availability of annotated fungal genomes and sophisticated bioinformatic software tools on the other hand, a detailed analysis of fungal secretomes has become feasible. While a number of reports on ascomycetous secretomes of, e.g., Aspergillus, Trichoderma, and Fusarium species are already available, studies on basidiomycetes have been mainly focused on the two model organisms Phanerochaete chrysosporium and Coprinopsis cinerea so far. Though an impressive number and diversity of fungal biocatalysts has been revealed by secretome analyses, the identity and function of many extracellular proteins still remains to be elucidated. A comprehensive understanding of the qualitative and quantitative composition of fungal secretomes, together with their synergistic actions and kinetic expression profiles, will allow for the development of optimized enzyme cocktails for white biotechnology.

This is a preview of subscription content, log in to check access.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Abbas A, Koc H, Liu F, Tien M (2005) Fungal degradation of wood: initial proteomic analysis of extracellular proteins of Phanerochaete chrysosporium grown on oak substrate. Curr Genet 47:49–56

  2. Aldarf M, Fourcade F, Amrane A, Prigent Y (2006) Substrate and metabolite diffusion within model medium for soft cheese in relation to growth of Penicillium camembertii. J Ind Microbiol Biotechnol 33:685–692

  3. Anh DH, Ullrich R, Scheibner K, Hofrichter M (2007) The coprophilous fungus Coprinus radians secretes a haloperoxidase that catalyzes aromatic peroxygenation. Appl Environ Microbiol 73:5477–5485

  4. Bertrand T, Jolivalt C, Caminade E, Joly N, Mougin C, Briozzo P (2001) Purification and preliminary crystallographic study of Trametes versicolor laccase in its native form. Acta Crystallogr 58:319–321

  5. Dwivedi RC (2006) Extracellular proteins from lignocellulose degrading basidiomycete: redox enzymes from Trametes versicolor and Coprinopsis cinerea. Ph.D. thesis, Georg-August-University Göttingen, Germany

  6. Glenn JK, Morgan MA, Mayfield MB, Kuwahara M, Gold MH (1983) An extracellular H2O2-requiring enzyme preparation involved in lignin biodegradation by the white rot basidiomycete Phanerochaete chrysosporium. Biochem Biophys Res Commun 114:1077–1083

  7. Guillen F, Martinez MJ, Munoz C, Martinez AT (1997) Quinone redox cycling in the ligninolytic fungus Pleurotus eryngii leading to extracellular production of superoxide anion radical. Arch Biochem Biophys 339:190–199

  8. Hamada N, Okumura R, Fuse N, Kodaira R, Shimosaka M, Kanda T, Okazaki M (1999) Isolation and transcriptional analysis of a cellulase gene (cel1) from the basidiomycete Irpex lacteus. J Ferment Bioeng 87:97–102

  9. Hatakka A (1994) Lignin-modifying enzymes from selected white-rot fungi: production and role in lignin degradation. FEMS Microbiol Rev 13:125–135

  10. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U (2006) Phylogenetic comparison and classification of laccase and related multi-copper oxidase protein sequences. FEBS J 273:2308–2326

  11. Hoegger PJ, Majcherczyk A, Dwivedi RC, Svobodova K, Kilaru S, Kües U (2008) Enzymes in wood degradation. In: Kües U (ed) Wood production, wood technology, and biotechnological impacts. Universitätsverlag Göttingen, Göttingen, Germany, pp 383–431

  12. Hofrichter M (2002) Review: lignin conversion by manganese peroxidase (MnP). Enzyme Microb Technol 30:454–466

  13. Hülsdau B (2007) Oxidativer Abbau von Carotinoiden durch Pilzenzyme. Ph.D. thesis, Leibniz University, Hannover, Germany

  14. Kawai R, Igarashi K, Yoshida M, Kitaoka M, Samejima M (2006) Hydrolysis of b-1,3/1,6-glucan by glycoside hydrolase family 16 endo-1,3(4)-b-glucanase from the basidiomycete Phanerochaete chrysosporium. Appl Microbiol Biotechnol 71:898–906

  15. Kilaru S, Hoegger PJ, Kües U (2006) The laccase multi-gene family in Coprinopsis cinerea has seventeen different members that divide into two distinct subfamilies. Curr Genet 50:45–60

  16. Kim Y, Nandakumar MP, Marten MR (2007) Proteomics of filamentous fungi. Trends Biotechnol 25:395–400

  17. Kim Y, Nandakumar MP, Marten MR (2008) The state of the proteome profiling in the fungal genus Aspergillus. Brief Funct Genomic Proteomic 7:87–94

  18. Kirk PM, Cannon PF, David JC, Stalpers J (2001) Ainsworth and Bisby’s dictionary of the fungi. CAB International, Wallingford, UK

  19. Klose J, Kobalz U (1995) Two-dimensional electrophoresis of proteins: an updated protocol and implications for a functional analysis of the genome. Electrophoresis 16:1034–1059

  20. Leonowicz A, Matuszewska A, Luterek J, Ziegenhagen D, Wojtas-Wasilewska M, Nam-Seok C, Hofrichter M, Rogalski J (1999) Biodegradation of lignin by white rot fungi. Fungal Genet Biol 27:175–185

  21. Linke D, Bouws H, Peters T, Nimtz M, Berger RG, Zorn H (2005) Laccases of Pleurotus sapidus: characterization and cloning. J Agric Food Chem 53(24):9498–9505

  22. Machida M, Asai K, Sano M, Tanaka T, Kumagai T, Terai G, Kusumoto K-I, Arima T, Akita O, Kashiwagi Y, Abe K, Gomi K, Horiuchi H, Kitamoto K, Kobayashi T, Takeuchi M, Denning DW, Galagan JE, Nierman WC, Yu J, Archer DB, Bennett JW, Bhatnagar D, Cleveland TE, Fedorova ND, Gotoh O, Horikawa H, Hosoyama A, Ichinomiya M, Igarashi R, Iwashita K, Rao Juvvadi P, Kato M, Kato Y, Kin T, Kokubun A, Maeda H, Maeyama N, Maruyama J-I, Nagasaki H, Nakajima T, Oda K, Okada K, Paulsen I, Sakamoto K, Sawano T, Takahashi M, Takase K, Terabayashi Y, Wortman JR, Yamada O, Yamagata Y, Anazawa H, Hata Y, Koide Y, Komori T, Koyama Y, Minetoki T, Suharnan S, Tanaka A, Isono K, Kuhara S, Ogasawara N, Kikuchi H (2005) Genome sequencing and analysis of Aspergillus oryzae. Nature 438:1157–1161

  23. Martinez D, Larrondo LF, Putnam N, Gelpke MD, Huang K, Chapman J, Helfenbein KG, Ramaiya P, Detter JC, Larimer F, Coutinho PM, Henrissat B, Berka R, Cullen D, Rokhsar D (2004) Genome sequence of the lignocellulose degrading fungus Phanerochaete chrysosporium strain RP78. Nat Biotechnol 22:679–680

  24. Martinez AT, Speranza M, Ruiz-Duenas FJ, Ferreira P, Camarero S, Guillen F, Martinez MJ, Gutierrez A, del Rio JC (2005) Biodegradation of lignocellulosics: microbial, chemical, and enzymatic aspects of the fungal attack of lignin. Int Microbiol 8:195–204

  25. Marzullo L, Cannio R, Giardina P, Santini MT, Sannia G (1995) Veratryl alcohol oxidase from Pleurotus ostreatus participates in lignin biodegradation and prevents polymerization of laccase-oxidized substrates. J Biol Chem 270:3823–3827

  26. Medina ML, Kiernan UA, Francisco WA (2004) Proteomic analysis of rutin-induced secreted proteins from Aspergillus flavus. Fungal Genet Biol 41:327–335

  27. Medina ML, Haynes PA, Breci L, Francisco WA (2005) Analysis of secreted proteins from Aspergillus flavus. Proteomics 5:3153–3161

  28. Oda K, Kakizono D, Yamada O, Iefuji H, Akita O, Iwashita K (2006) Proteomic analysis of extracellular proteins from Aspergillus oryzae grown under submerged and solid-state culture conditions. Appl Environ Microbiol 72:3448–3457

  29. O’Farrell PH (1975) High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250:4007–4021

  30. Paper JM, Scott-Craig JS, Adhikari ND, Cuomo CA, Walton JD (2007) Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 7:3171–3183

  31. Ruiz-Duenas FJ, Martinez MJ, Martinez AT (1999) Molecular characterization of a novel peroxidase isolated from the ligninolytic fungus Pleurotus eryngii. Mol Microbiol 31:223–235

  32. Sato S, Liu F, Koc H, Tien M (2007) Expression analysis of extracellular proteins from Phanerochaete chrysosporium grown on different liquid and solid substrates. Microbiology 153:3023–3033

  33. Scheibner M, Hülsdau B, Zelena K, Nimtz M, de Boer L, Berger RG, Zorn H (2007) Novel peroxidases of Marasmius scorodonius degrade b-carotene. Appl Microbiol Biotechnol 77:1241–1250

  34. Shu CH, Xu CJ, Lin ES (2006) Production, purification and partial characterization of a novel endo-b-1,3-glucanase from Agaricus brasiliensis. Process Biochem 41:1229–1233

  35. Steinbüchel A (2006) Nachwachsende rohstoffe für die weiße biotechnologie. In: Heiden S, Zinke H (eds) Weiße biotechnologie—industrie im Aufbruch. Biocom AG, Berlin, pp 76–91

  36. Suárez MB, Sanz L, Chamorro MI, Rey M, González FJ, Llobell A, Monte E (2005) Proteomic analysis of secreted proteins from Trichoderma harzianum. Identification of a fungal cell wall-induced aspartic protease. Fungal Genet Biol 42:924–934

  37. Tjalsma H, Bolhuis A, Jongbloed JDH, Bron S, van Dijl JM (2000) Signal peptide-dependent protein transport in Bacillus subtilis: a genome-based survey of the secretome. Microbial Mol Biol Rev 64:515–547

  38. Valášková V, Baldrian P (2006) Degradation of cellulose and hemicellulose by the brown rot fungus Piptoporus betulinus—production of extracellular enzymes and characterization of the major cellulases. Microbiology 152:3613–3622

  39. van den Berg MA, Westerlaken I, Leeflang C, Kerkman R, Bovenberg RAL (2007) Functional characterization of the penicillin biosynthetic gene cluster of Penicillium chrysogenum Wisconsin 54-1255. Fungal Genet Biol 44:830–844

  40. Vanden Wymelenberg A, Sabat G, Martinez D, Rajangam AS, Tuula TT, Gaskell J, Kersten PJ, Cullen D (2005) The Phanerochaete chrysosporium secretome: database predictions and initial mass spectrometry peptide identifications in cellulose-grown medium. J Biotechnol 118:17–34

  41. Vanden Wymelenberg A, Minges P, Sabat G, Martinez D, Aerts A, Salamov A, Grigoriev I, Shapiro H, Putnam N, Belinky P, Dosoretz C, Gaskell J, Kersten PJ, Cullen D (2006) Computational analysis of the Phanerochaete chrysosporium v2.0 genome database and mass spectrometry identification of peptides in ligninolytic cultures reveal complex mixtures of secreted proteins. Fungal Genet Biol 43:343–356

  42. Vares T, Kalsi M, Hatakka A (1995) Lignin peroxidases, manganese peroxidases, and other ligninolytic enzymes produced by Phlebia radiata during solid-state fermentation of wheat straw. Appl Environ Microbiol 61:3515–3520

  43. Vinzant TB, Adney WS, Decker SR, Baker JO, Kinter MT, Sherman NE, Fox JW, Himmel ME (2001) Fingerprinting Trichoderma reesei hydrolases in a commercial cellulase preparation. Appl Biochem Biotechnol 91:99–107

  44. Weingarten P, Lutter P, Wattenberg A, Blueggel M, Bailey S, Klose J, Meyer HE, Huels C (2005) Application of proteomics and protein analysis for biomarker and target finding for immunotherapy. Methods Mol Med 109:155–173

  45. Xiao YZ, Tu XM, Wang J, Zhang M, Cheng Q, Zeng WY, Shi YY (2003) Purification, molecular characterization and reactivity with aromatic compounds of a laccase from basidiomycete Trametes sp strain AH28-2. Appl Microbiol Biotechnol 60:700–707

  46. Yajina W, Kav NNV (2006) The proteome of the phytopathogenic fungus Sclerotinia sclerotium. Proteomics 6:5995–6007

  47. Yates JR, Eng JK, McCormack AL, Schieltz D (1995) Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 67:1426–1436

  48. Yaver DS, Overjero MDC, Xu F, Nelson BA, Brown KM, Halkier T, Bernauer S, Brown SH, Kauppinen S (1999) Molecular characterization of laccase genes from the basidiomycete Coprinus cinereus and heterologous expression of the laccase Lcc1. Appl Environ Microbiol 65:4943–4948

  49. Zorn H, Bouws H, Takenberg M, Nimtz M, Getzlaff R, Breithaupt D, Berger RG (2005a) An extracellular carboxylesterase from the basidiomycete Pleurotus sapidus hydrolyses xanthophyll esters. Biol Chem 386:435–440

  50. Zorn H, Peters T, Nimtz M, Berger RG (2005b) The secretome of Pleurotus sapidus. Proteomics 5:4832–4838

Download references

Acknowledgments

Financial support of the project “Fungal secretomes for the efficient degradation of lignocelluloses” (AZ 13199-32) by the “Deutsche Bundesstiftung Umwelt, DBU” is gratefully acknowledged.

Author information

Correspondence to Holger Zorn.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bouws, H., Wattenberg, A. & Zorn, H. Fungal secretomes—nature’s toolbox for white biotechnology. Appl Microbiol Biotechnol 80, 381 (2008). https://doi.org/10.1007/s00253-008-1572-5

Download citation

Keywords

  • Ascomycetes
  • Basidiomycetes
  • 2-D electrophoresis
  • Tandem-mass spectrometry