Skip to main content
SpringerLink
Log in

Lignocellulosic polysaccharides and lignin degradation by wood decay fungi: the relevance of nonenzymatic Fenton-based reactions

  • Original Paper
  • Published:
Journal of Industrial Microbiology & Biotechnology

Abstract

The brown rot fungus Wolfiporia cocos and the selective white rot fungus Perenniporia medulla-panis produce peptides and phenolate-derivative compounds as low molecular weight Fe3+-reductants. Phenolates were the major compounds with Fe3+-reducing activity in both fungi and displayed Fe3+-reducing activity at pH 2.0 and 4.5 in the absence and presence of oxalic acid. The chemical structures of these compounds were identified. Together with Fe3+ and H2O2 (mediated Fenton reaction) they produced oxygen radicals that oxidized lignocellulosic polysaccharides and lignin extensively in vitro under conditions similar to those found in vivo. These results indicate that, in addition to the extensively studied Gloeophyllum trabeum—a model brown rot fungus—other brown rot fungi as well as selective white rot fungi, possess the means to promote Fenton chemistry to degrade cellulose and hemicellulose, and to modify lignin. Moreover, new information is provided, particularly regarding how lignin is attacked, and either repolymerized or solubilized depending on the type of fungal attack, and suggests a new pathway for selective white rot degradation of wood. The importance of Fenton reactions mediated by phenolates operating separately or synergistically with carbohydrate-degrading enzymes in brown rot fungi, and lignin-modifying enzymes in white rot fungi is discussed. This research improves our understanding of natural processes in carbon cycling in the environment, which may enable the exploration of novel methods for bioconversion of lignocellulose in the production of biofuels or polymers, in addition to the development of new and better ways to protect wood from degradation by microorganisms.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Arantes V, Milagres AMF (2007) The synergistic action of ligninolytic enzymes (MnP and Laccase) and Fe3+-reducing activity from white-rot fungi for degradation of Azure B. Enzyme Microb Technol 42:17–22

    Article  CAS  Google Scholar 

  2. Arantes V, Milagres AMF (2007) The effect of a catecholate chelator as a redox agent in Fenton-based reactions on degradation of lignin model substrates and on COD removal from effluent of an ECF kraft pulp mill. J Hazard Mater 141:273–279

    Article  PubMed  CAS  Google Scholar 

  3. Arantes V, Milagres AMF (2007) Application of statistical experimental design to the treatment of bleaching kraft mill effluent using a mediated free radical system. Water Sci Technol 55:1–7

    PubMed  Google Scholar 

  4. Arantes V, Baldochi C, Milagres AMF (2006) Degradation and decolorization of a biodegradable-resistant polymeric dye by chelator-mediated Fenton reactions. Chemosphere 63:1764–1772

    Article  PubMed  CAS  Google Scholar 

  5. Wesenberg D, Kyriakides I, Agathos SN (2003) White-rot fungi and their enzymes for the treatment of industrial dye effluents. Biotechnol Adv 22:161–187

    Article  PubMed  CAS  Google Scholar 

  6. Duran N, Esposito E (2000) Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment: a review. Appl Catal B Environ 28:83–99

    Article  CAS  Google Scholar 

  7. Alam MZ, Kabbashi NA, Hussin SNIS (2009) Production of bioethanol by direct bioconversion of oil-palm industrial effluent in a stirred-tank bioreactor. J Ind Microbiol Biotechnol 36:801–808

    Article  PubMed  CAS  Google Scholar 

  8. Lee JW, Koo BW, Choi JW, Choi DH, Choi IG (2008) Evaluation of waste mushroom logs as a potential biomass resource for the production of bioethanol. Bioresour Technol 99:2736–2741

    Article  PubMed  CAS  Google Scholar 

  9. Ferraz A, Guerra A, Mendonça R, Masarin F, Vicentim MP, Aguiar A, Pavan PC (2008) Technological advances and mechanistic basis for fungal biopulping. Enzyme Microb Technol 43:178–185

    Article  CAS  Google Scholar 

  10. Moreira MT, Feijoo G, Canaval J, Lema JM (2003) Semipilot-scale bleaching of kraft pulp with manganese peroxide. Wood Sci Technol 37:117–1234

    Article  CAS  Google Scholar 

  11. Milagres AMF, Arantes V, Medeiros CL, Machuca A (2002) Production of metal chelating compounds by white and brown-rot fungi and their comparative abilities for pulp bleaching. Enzyme Microb Technol 30:562–565

    Article  CAS  Google Scholar 

  12. Qian Y, Goodell B, Genco JM (2002) The effect of a chelator-mediated Fenton system on the fiber and paper properties of hardwood Kraft pulp. J Wood Chem Technol 22:267–284

    Article  CAS  Google Scholar 

  13. Archibald FS, Bourbonnais R, Jurasek L, Paice MG, Reid ID (1997) Kraft pulp bleaching and delignification by Trametes versicolor. Appl Environ Microbiol 58:3101–3109

    Google Scholar 

  14. Kondo R, Kurashiki K, Sakai K (1994) Bleaching of hardwood kraft pulp with manganese peroxidase secreted from Phanerochaete sordita YK-624. Appl Environ Microbiol 60:4359–4363

    PubMed  CAS  Google Scholar 

  15. Isildak O, Turkekul I, Elmastas M, Tuzen M (2004) Analysis of heavy metals in some wild-grown edible mushrooms from the middle black sea region, Turkey. Food Chem 86:547–552

    Article  CAS  Google Scholar 

  16. Gübitza GM, Mansfield SD, Böhma D, Saddler JN (1998) Effect of endoglucanases and hemicellulases in magnetic and flotation deinking of xerographic and laser-printed papers. J Biotechnol 65:209–215

    Article  Google Scholar 

  17. Qian Y, Goodell B (2005) Deinking of laser printed copy paper with a mediated free radical system. Bioresour Technol 96:913–920

    Article  PubMed  CAS  Google Scholar 

  18. Job-Cei C, Keller J, Job D (1996) Degradation of unbleached pulp paper treated in solid state conditions with five species of the brown rot Gloeophyllum. Mater Organismen 30:105–116

    CAS  Google Scholar 

  19. Qian Y, Goodell B, Jellison J, Felix CC (2004) The effect of hydroxyl radical generation on free-radical activation of TMP fibers. J Polym Environ 12:147–155

    Article  CAS  Google Scholar 

  20. Blanchette RA, Krueger EW, Haight JE, Akhtar M, Akin DE (1997) Cell wall alterations in loblolly pine wood decayed by the white-rot fungus, Ceriporiopsis subvermispora. J Biotechnol 53:203–213

    Article  CAS  Google Scholar 

  21. Goodell B, Jellison J, Liu J, Daniel G, Paszczynski A, Fekete F, Krishnamurthy S, Jun L, Xu G (1997) Low molecular weight chelators and phenolic compounds isolated from wood decay fungi and their role in the fungal biodegradation of wood. J Biotechnol 53:133–162

    Article  CAS  Google Scholar 

  22. Poulos TL, Edwards SL, Wariishi H, Gold MH (1993) Crystallographic refinement of lignin peroxidase at 2 A. J Biol Chem 268:4429–4440

    PubMed  CAS  Google Scholar 

  23. Guerra A, Mendonça R, Ferraz A (2003) Molecular weight distribution of wood components extracted from Pinus taeda biotreated by Ceriporiopsis subvermispora. Enzyme Microb Technol 33:12–18

    Article  CAS  Google Scholar 

  24. Arantes V, Milagres AMF (2009) The relevance of low molecular weight compounds in wood biodegradation by fungi. Quim Nova 30:1586–1595

    Google Scholar 

  25. Bourbonnais R, Paice MG (1990) Oxidation of non-phenolic substrates: an expanded role for laccase in lignin biodegradation. FEBS Lett 26:99–102

    Article  Google Scholar 

  26. ten Have R, Teunissen PJM (2001) Oxidative mechanisms involved in lignin degradation by white-rot fungi. Chem Rev 101:3397–3413

    Article  PubMed  CAS  Google Scholar 

  27. Daniel G (2003) Microview of wood under degradation by bacteria and fungi. In: Goodell B, Nicholas DD, Schultz TP (eds) Wood deterioration and preservation: advances in our changing world. ACS Symposium Series 845, Washington, DC, pp 34–72

    Chapter  Google Scholar 

  28. Jellison J, Chandhoke V, Goodell B, Fekete FA (1991) The isolation and immunolocalization of iron-binding compounds produced by Gloeophyllum traveum. Appl Microbiol Biotechnol 35:805–809

    Article  CAS  Google Scholar 

  29. Hammel KE, Kapich AN, Jensen KA Jr, Ryan ZC (2002) Reactive oxygen species as agents of wood decay by fungi. Enzyme Microb Technol 30:445–453

    Article  CAS  Google Scholar 

  30. Enoki A, Itajura S, Tanaka H (1997) The involvement of extracelullar substances for reducing molecular oxygen to hydroxyl radical and ferric ion to ferrous iron in wood degradation by wood decay fungi. J Biotechnol 53:265–272

    Article  CAS  Google Scholar 

  31. Wang W, Gao PJ (2003) Function and mechanism of a low-molecular-weight peptide produced by Gleophyllum trabeum in biodegradation of cellulose. J Biotechnol 101:119–130

    Article  PubMed  Google Scholar 

  32. Goodell B (2003) Brown rot degradation of wood: our evolving view In: Goodell B, Nicholas DD, Schultz TP (eds) Wood deterioration and preservation: advances in our changing world. ACS Symposium Series 845, Washington, DC, pp 97–118

  33. Arantes V, Milagres AMF (2006) Degradation of cellulosic and hemicellulosic substrates using a chelator-mediated Fenton reaction. J Chem Technol Biotechnol 81:413–419

    Article  CAS  Google Scholar 

  34. Paszczynski A, Crawford R, Funk D, Goodell B (1999) The novo synthesis of 4, 5-dimethoxycatechol and 2, 5-dimethoxyhydroquinone by the brown rot fungus Gloeophyllum trabeum. Appl Environ Microbiol 65:674–679

    PubMed  CAS  Google Scholar 

  35. Jensen KA, Houtman CJ, Ryan ZC, Hammel KE (2001) Pathways for extracellular Fenton chemistry in the brown rot basidiomycete Gloeophyllum trabeum. Appl Microbiol Biotechnol 67:2705–2711

    CAS  Google Scholar 

  36. Varela W, Tien M (2003) Effect of pH and oxalate on hydroquinone-derived hydroxyl radical formation during brown rot wood degradation. Appl Environ Microbiol 69:6025–6031

    Article  PubMed  CAS  Google Scholar 

  37. Cohen R, Jensen KA, Houtman CJ, Hammel KE (2002) Significant levels of extracellular reactive oxygen species produced by brown rot basidiomycetes on cellulose. FEBS Lett 531:483–488

    Article  PubMed  CAS  Google Scholar 

  38. Xu G, Goodell B (2001) Mechanism of wood degradation by brown-rot fungi: chelator-mediated cellulose degradation and binding of iron by cellulose. J Biotechnol 27:43–57

    Article  Google Scholar 

  39. Arantes V, Milagres AMF (2006) Evaluation of different carbon sources for production of iron-reducing compounds by Wolfiporia cocos and Perenniporia medulla-panis. Process Biochem 41:887–891

    Article  CAS  Google Scholar 

  40. Simionato A, Simó C, Cifuentes A, Lacava PT, Araújo WL, Azevedo JL, Carrilho E (2006) Capillary electrophoresis-mass spectrometry of citrus endophytic bacteria siderophores. Electrophoresis 27:2567–2574

    Article  PubMed  CAS  Google Scholar 

  41. Jiang L, He L, Fountoulakis M (2004) Comparison of protein precipitation methods for sample preparation prior to proteomic analysis. J Chromatogr A 1023:317–320

    Article  PubMed  CAS  Google Scholar 

  42. Stookey L (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42:781–783

    Article  Google Scholar 

  43. Arnow LE (1937) Colorimetric determination of the components of 3, 4-dihydroxyphenylalanine-tyrosine mixtures. J Biol Chem 118:531–537

    CAS  Google Scholar 

  44. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    PubMed  CAS  Google Scholar 

  45. Filley TR, Minard RD, Hatcher PG (1999) Tetramethylammonium hydroxide (TMAH) thermochemolysis: proposed mechanisms based on the application of 13C-labeled TMAH to a synthetic model lignin dimmer. Org Geochem 30:607–621

    Article  CAS  Google Scholar 

  46. Kalogeris E, Christakopoulos P, Kekos D, Macris BJ (1998) Studies on the solid-state production of thermostable endoxylanases from Thermoascus aurantiacus: characterization of two isozymes. J Biotechnol 60:155–163

    Article  CAS  Google Scholar 

  47. Arantes V, Qian Y, Kelley SS, Milagres AMF, Filley TR, Jellison J, Goodell B (2009) Biomimetic oxidative treatment of spruce wood studied by pyrolysis–molecular beam mass spectrometry coupled with multivariate analysis and 13C-labeled tetramethylammonium hydroxide thermochemolysis: implications for fungal degradation of wood. J Biol Inorg Chem 8:1253–1263

    Article  Google Scholar 

  48. Filley TR, Nierop KGJ, Wang Y (2006) The contribution of polyhydroxyl aromatic compounds to tetramethylammonium hydroxide lignin-based proxies. Org Geochem 37:711–727

    Article  CAS  Google Scholar 

  49. Schmidt CJ, Whitten BK, Nicholas DD (1981) A proposed role for oxalic acid in non-enzymatic wood decay by brown-rot fungi. Am Wood Presev Assoc 77:157–164

    Google Scholar 

  50. Arantes V, Qian Y, Milagres AMF, Jellison J, Goodell B (2009) Effect of pH and oxalic acid on the reduction of Fe3+ by a biomimetic chelator and on Fe3+ desorption/adsorption onto wood: Implications for brown rot decay. Int Biodeterioration Biodegr 63:478–483

    Article  CAS  Google Scholar 

  51. Schilling JS, Jellison J (2005) Oxalate regulation by two brown rot fungi decaying oxalate-amended and non-amended wood. Holzforschung 59:681–688

    Article  CAS  Google Scholar 

  52. Connolly J, Jellison J (1995) Calcium translocation, calcium oxalate accumulation, and hyphal sheath morphology in the white-rot fungus Resinicium bicolor. Can J Bot 73:927–936

    CAS  Google Scholar 

  53. Clausen CA, Green F III (2003) Oxalic acid overproduction by copper-tolerant brown-rot basidiomycetes on southern yellow pine treated with copper-based preservatives. Int Biodeterioration Biodegr 51:138–144

    Google Scholar 

  54. Aguiar A, Ferraz A (2007) Fe3+- and Cu2+-reduction by phenol derivatives associated with Azure B degradation in Fenton-like reactions. Chemosphere 66:947–954

    Article  PubMed  CAS  Google Scholar 

  55. Kamnev AA, Kuzmann E (1997) Mossbaurer spectroscopic evidence for the reduction of iron (III) by anthranilic acid in aqueous solution. Polyhedron 16:3353–3356

    Article  CAS  Google Scholar 

  56. Gutiérrez A, Del Rio JC, Martinez-Inigo MJL, Martinez MJ, Martinez AT (2002) Production of new unsaturated lipids during wood decay by ligninolytic basidiomycetes. Appl Environ Microbiol 68:1344–1350

    Article  PubMed  Google Scholar 

  57. de Jong E, Field JA, Spinnler HE, Wijnberg JBPA, de Bont JAM (1994) Significant biogenesis of chlorinated aromatics by fungi in natural environments. Appl Environ Microbiol 60:264–270

    PubMed  Google Scholar 

  58. Ortiz-Bermúdez P, Hirth KC, Srebotnik E, Hammel KE (2007) Chlorination of lignin by ubiquitous fungi has a likely role in global organochlorine production. Proc Natl Acad Sci USA 104:3895–3900

    Article  PubMed  Google Scholar 

  59. Teunissen PJ, Sheng D, Reddy GV, Moenne-Loccoz P, Field JA, Gold MH (1998)  2-Chloro-1, 4-dimethoxybenzene cation radical: formation and role in the lignin peroxidase oxidation of anisyl alcohol. Arch Biochem Biophys 360:233–238

    Article  PubMed  CAS  Google Scholar 

  60. Milagres AMF, Sales R (2001) Evaluating the basidiomycetes Poria medula-panis and Wolfiporia cocos for xylanase production. Enzyme Microb Technol 28:522–526

    Article  PubMed  CAS  Google Scholar 

  61. Machuca A, Ferraz A (2001) Hydrolytic and oxidative enzymes produced by white and brown-rot fungi during Eucalyptus grandis decay in solid medium. Enzme Microb Technol 29:386–391

    Article  CAS  Google Scholar 

  62. Coughlan MP (1985) The properties of fungal and bacterial cellulases with comment on their production and application. In: Russell GE (ed) Biotechnology and genetic engineering reviews, v 3. Interscience, Newcastle-upon-Tyne, pp 37–109

    Google Scholar 

  63. Arantes V, Saddler JN (2010) Access to cellulose limits the efficiency of enzymatic hydrolysis: the role of amorphogenesis. Biotechnol Biofuel 3:4

    Article  Google Scholar 

  64. Reese ET, Sui RGH, Levinson HS (1950) The biological degradation of soluble cellulose derivatives and its relationship to the mechanisms of cellulose hydrolysis. J Bacteriol 59:485–497

    PubMed  CAS  Google Scholar 

  65. Mandels M, Reese ET (1964) Fungal cellulases and the microbial decomposition of cellulosic fabric. Dev Ind Mycol 5:5–20

    CAS  Google Scholar 

  66. Filley TR, Hatcher PG, Shortle WC, Praseuth RT (2000) The application of 13C-labeled tetramethylammonium hydroxide (13C-TMAH) thermochemolysis to the study of fungal degradation of wood. Org Geochem 31:181–198

    Article  CAS  Google Scholar 

  67. Highley TL, Dashek WV (1998) Biotechnology in the study of brown- and white-rot decay. In: Bruce A, Palfreyman JW (eds) Forest products biotechnology. Taylor & Francis, London, pp 15–36

    Google Scholar 

  68. Filley TR, Cody GD, Goodell B, Jellison J, Noser C, Ostrofsky A (2002) Lignin demethylation and polysaccharide decomposition in spruce sapwood degraded by brown rot fungi. Org Geochem 33:111–124

    Article  CAS  Google Scholar 

  69. Vane CH, Martin SC, Snape CE, Abbott GD (2001) Degradation of lignin in wheat straw during growth of the oyster mushroon Pleurotus ostreatus using off-line thermochemolysis with tetramethylammonium hydroxide and solid state 13C NMR. J Agr Food Chem 49:2709–2716

    Article  CAS  Google Scholar 

  70. Hammel KE, Jensen KA, Mozuch MD, Landucci LL, Tien M, Pease EA (1993) Ligninolysis by a purified lignin peroxidase. J Biol Chem 268:12274–12281

    PubMed  CAS  Google Scholar 

  71. Schuerch C (1952) The solvent properties of liquids and their relation to the solubility, swelling, isolation and fractionation of lignin. J Am Chem Soc 74:5061–5067

    Article  CAS  Google Scholar 

  72. Tanaka H, Itakura S, Enoki A (1999) Hydroxyl radical generation by an extracellular low-molecular-weight substance and phenol oxidase activity during wood degradation by the white-rot basidiomycete Trametes versicolor. J Biotechnol 75:57–70

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the State of São Paulo Research Foundation (FAPESP, Brazil) Grant 04/12080-0 and 07/00993-9. V.A. is also grateful to the Coordination for the Improvement of Higher Level Personnel (CAPES-Brazil) Grant No. 5192/06-4 for the financial support for his stay at the Sustainable Biomaterials and Bioenergy/Wood Science Laboratories at the University of Maine, Orono-ME/USA and we thank the University of Maine Wood Utilization Research (WUR) program for laboratory support.

Author information

Authors and Affiliations

  1. Forestry Products Biotechnology/Bioenergy Group, Department of Wood Science, Faculty of Forestry, University of British Columbia, 2424 Main Mall, Vancouver, BC, V6T 1Z4, Canada

    Valdeir Arantes

  2. Department of Biotechnology, Escola de Engenharia de Lorena, University of São Paulo, Lorea, SP, Brazil

    Adriane M. F. Milagres

  3. Department of Earth and Atmospheric Sciences, Purdue University, West Lafayette, IN, USA

    Timothy R. Filley

  4. Sustainable Biomaterials and Bioenergy (SFR)/Wood Science, University of Maine, Orono, ME, USA

    Barry Goodell

Authors
  1. Valdeir Arantes
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adriane M. F. Milagres
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Timothy R. Filley
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Barry Goodell
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valdeir Arantes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Arantes, V., Milagres, A.M.F., Filley, T.R. et al. Lignocellulosic polysaccharides and lignin degradation by wood decay fungi: the relevance of nonenzymatic Fenton-based reactions. J Ind Microbiol Biotechnol 38, 541–555 (2011). https://doi.org/10.1007/s10295-010-0798-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10295-010-0798-2

Keywords

Search

Navigation