Skip to main content

Official Journal of the Japan Wood Research Society

  • Original Article
  • Published:

Glyoxal oxidase supplies hydrogen peroxide at hyphal tips and on hyphal wall to manganese peroxidase of white-rot fungus Phanerochaete crassa WD1694

Abstract

Peroxidase activity staining localized at hyphal tips of white-rot fungus Phanerochaete crassa WD1694 that was cultivated in a shaken liquid culture containing unbleached kraft pulp was investigated. Manganese peroxidase was detected in culture solution, washing solution of mycelium, and mycelial extract. Glyoxal oxidase was detected only in mycelial extract and was not detected in culture solution. Addition of hydrogen peroxide generated peroxidase activity staining in the culture solution. Addition of catalase resulted in no staining in the culture of P. crassa WD1694, and the addition of methylglyoxal resulted in marked peroxidase activity staining at hyphal tips and on hyphal wall. In an optimized culture, glyoxal oxidase was produced in culture solution. Although the production of glyoxal oxidase and manganese peroxidase had a positive correlation, the secretion and the peak of glyoxal oxidase was observed 3 and 2 days later than those of manganese peroxidase. The N-terminal sequence of purified glyoxal oxidase had very high homology with that of P. chrysosporium. These results elucidated the hydrogen peroxide supply system in lignin biodegradation by white-rot fungi, i.e., while remaining on the hyphal cell wall, glyoxal oxidase provides hydrogen peroxide to manganese peroxidase that had diffused into the culture solution beforehand.

References

  1. Nakano J (1979) Lignin in plants (in Japanese). In: Nakano J (ed) Chemistry of lignin, basic science and application. Uni, Tokyo, pp 20–36

    Google Scholar 

  2. Higuchi T (1985) Biosynthesis of lignin. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic, London, pp 141–161

    Google Scholar 

  3. Chen CL, Chang HM (1985) Chemistry of lignin biodegradation. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic, London, pp 535–556

    Google Scholar 

  4. Ander P (1990) Biodegradation of lignin. In: Eriksson KEL, Blanchette RA, Ander P (eds) Microbial and enzymatic degradation of wood and wood components. Springer-Verlag, Berlin, pp 225–333

    Google Scholar 

  5. Barz W, Weltring KM (1985) Biodegradation of aromatic extractives of wood. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic, London, pp 607–666

    Google Scholar 

  6. Higuchi T (1985) Degradative pathways of lignin model compounds. In: Higuchi T (ed) Biosynthesis and biodegradation of wood components. Academic, London, pp 557–578

    Google Scholar 

  7. Umezawa T (1988) Mechanisms for chemical reactions involved in lignin biodegradation by Phanerochaete chrysosporium. Wood Res 75:21–79

    CAS  Google Scholar 

  8. 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

    Article  PubMed  CAS  Google Scholar 

  9. Kuwahara M, Glenn JK, Morgan MA, Gold MH (1984) Separation and characterization of two extracellular H2O2-dependent oxidases from ligninolytic cultures of Phanerochaete chrysosporium. FEBS Lett 169:247–250

    Article  CAS  Google Scholar 

  10. Tien M, Kirk TK (1983) Lignin-degrading enzyme from the hymenomycete Phanerochaete chrysosporium burds. Science 221:661–663

    Article  PubMed  CAS  Google Scholar 

  11. Gold MH, Alic M (1993) Molecular biology of the lignin-degrading basidiomycete Phanerochaete chrysosporium. Microbiol Rev 57:605–622

    PubMed  CAS  Google Scholar 

  12. Kirk TK (1987) Enzymatic “combustion”: the microbial degradation of lignin. Ann Rev Microbiol 41:465–505

    Article  CAS  Google Scholar 

  13. Gold MH, Wariishi H, Valli K (1989) Extracellular peroxidases involved in lignin degradation by the white rot basidiomycete Phanerochaete chrysosporium. In: Biocatalysis in agricultural biotechnology. ACS, Washington, DC, pp 127–140

    Chapter  Google Scholar 

  14. Daniel G (1994) Use of electron microscopy for aiding our understanding of wood biodegradation. FEMS Microbial Rev 13:199–233

    Article  CAS  Google Scholar 

  15. Daniel G, Nilsson T, Pettersson B (1989) Intra- and extracellular localization of lignin peroxidase during the degradation of solid wood and wood fragments by Phanerochaete chrysosporium by using transmission electron microscopy and immuno-gold labeling. Appl Environ Microbiol 55:871–881

    PubMed  CAS  Google Scholar 

  16. Joseleau JP, Ruel K (1992) Ultrastructural examination of lignin and polysaccharide degradation in wood by white-rot fungi. In: Kuwahara M, Shimada M (eds) Biotechnology in pulp and paper industry. Uni, Tokyo, pp 195–201

    Google Scholar 

  17. Daniel G, Pettersson B, Volc J, Nilsson T (1990) Spatial distribution of lignin- and manganese peroxidase(s) during degradation of wood and wood fragments by Phanerochaete chrysosporium as revealed by T.E.M. immunogold labeling. In: Kirk TK, Chang H-M (eds) Biotechnology in pulp and paper manufacture, applications and fundamental investigations. Butterworth-Heinemann, Woburn, pp 99–110

    Google Scholar 

  18. Takano M, Abe H, Hayashi N (2006) Extracellular peroxidase activity at the hyphal tips of the white-rot fungus Phanerochaete crassa WD1694. J Wood Sci 52:429–435

    Article  CAS  Google Scholar 

  19. Takano M, Hayashi N, Nakamura M, Yamaguchi M (2009) Extracellular peroxidase reaction at hyphal tips of white-rot fungus Phanerochaete crassa WD1694 and in fungal slime. J Wood Sci 55:302–307

    Article  CAS  Google Scholar 

  20. Takano M, Nishida A, Nakamura M (2001) Screening of wood-rotting fungi for kraft pulp bleaching by the Poly R decoloration test and biobleaching of hardwood kraft pulp by Phanerochaete crassa WD1694. J Wood Sci 47:63–68

    Article  CAS  Google Scholar 

  21. Gold MH, Glenn JK (1988) Manganese peroxidase from Phanerochaete chrysosporium. In: Wood WA, Kellogg ST (eds) Methods in enzymology, 161 part B. Academic, New York, pp 258–264

    Google Scholar 

  22. Kersten PJ (1990) Glyoxal oxidase of Phanerochaete chrysosporium: Its characterization and activation by lignin peroxidase. Proc Natl Acad Sci USA 87:2936–2940

    Article  PubMed  CAS  Google Scholar 

  23. Kersten PJ, Kirk TK (1987) Involvement of a new enzyme, glyoxal oxidase, in extracellular H2O2 production by Phanerochaete chrysosporium. J Biol Chem 169:2195–2201

    CAS  Google Scholar 

  24. Kelley RL, Reddy CA (1986) Purification and characterization of glucose oxidase from ligninolytic cultures of Phanerochaete chrysosporium. J Bacteriol 166:269–274

    PubMed  CAS  Google Scholar 

  25. Kelley RL, Reddy CA (1986) Identification of glucose oxidase activity as the primary source of hydrogen peroxide in ligninolytic cultures of Phanerochaete chrysosporium. Arch Microbiol 144:248–253

    Article  CAS  Google Scholar 

  26. Eriksson KE, Pettersson B, Volc J, Musilek V (1986) Formation and partial characterization of glucose-2-oxidase, a H2O2-producing enzyme in Phanerochaete chrysosporium. Appl Microbiol Biotechnol 23:257–262

    Article  CAS  Google Scholar 

  27. Guillen F, Martinez AT, Martinez MJ (1990) Production of hydrogen peroxide by aryl-alcohol oxidase from the ligninolytic fungus Pleurotus eryngii. Appl Micro Biotechnol 32:465–469

    Article  CAS  Google Scholar 

  28. Nishida A, Eriksson KE (1987) Formation, purification and partial characterization of methanol oxidase, a H2O2-producing enzyme in Phanerochaete chrysosporium. Biotechnol Appl Biochem 9:325–338

    CAS  Google Scholar 

  29. Kersten PJ, Cullen D (1993) Cloning and characterization of a cDNA encoding glyoxal oxidase, a H2O2-producing enzyme from the lignin-degrading basidiomycete Phanerochaete chrysosporium. Proc Natl Acad Sci USA 90:7411–7413

    Article  PubMed  CAS  Google Scholar 

  30. Takano M, Nakamura M, Nishida A, Ishihara M (2004) Manganese peroxidase from Phanerochaete crassa WD1694. Bull For For Prod Res Inst 3:7–13

    CAS  Google Scholar 

  31. Wösten HAB, Moukha SM, Siestsma JH, Wessels JGH (1991) Localization of growth and secretion of proteins in Aspergillus niger. J Microbiol 137:2017–2023

    Article  Google Scholar 

  32. Wessels JGH (1993) Wall growth, protein secretion and morphogenesis in fungi. New Phytol 123:3970413

    Article  Google Scholar 

  33. Cai YJ, Chapman SJ, Buswell JA, Chang S (1999) Production and distribution of endoglucanase, cellobiohydrolase, and β-glucosidase components of the cellulolytic system of Volvariella volvacea, the edible straw mushroom. Appl Environ Microbiol 65:553–559

    PubMed  CAS  Google Scholar 

  34. Buswell JA, Odier E (1987) Lignin biodegradation. CRC Crit Rev Biotechnol 6:1–60

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Mariko Takano.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Takano, M., Nakamura, M. & Yamaguchi, M. Glyoxal oxidase supplies hydrogen peroxide at hyphal tips and on hyphal wall to manganese peroxidase of white-rot fungus Phanerochaete crassa WD1694. J Wood Sci 56, 307–313 (2010). https://doi.org/10.1007/s10086-009-1105-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10086-009-1105-6

Key words