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References

  1. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U. 2006. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J. 273:2308-2326.
    Pubmed CrossRef
  2. Rivera-Hoyos CM, Morales-Álvarez ED, Poutou-Piñales RA, Pedroza-Rodríjuez AM, Rodríguez-Vázquez R, DelgadoBoada JM. 2013. Fungal laccases. Fungal Biol. Rev. 27: 67-82.
    CrossRef
  3. Bajpai P. 1999. Application of enzymes in the pulp and paper industry. Biotechnol. Prog. 15: 147-157.
    Pubmed CrossRef
  4. Durán N, Rosa MA, D’Annibale A, Gianfreda L. 2002. Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzyme Microb. Technol. 31: 907-931.
    CrossRef
  5. Cameselle C, Pazos M, Lorenzo M, Sanromán MA. 2003. Enhanced decolourisation ability of laccase towards various synthetic dyes by an electrocatalysis technology. Biotechnol. Lett. 25: 603-606.
    Pubmed CrossRef
  6. Rim K, Lasssd B, Steve W, Mariem E, Abdelhafidh D, Sarni S, Tabar M. 2010. Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J. Hazard. Mater. 175: 802-808.
    Pubmed CrossRef
  7. Levin L, Melignani E, Ramos AM. 2010. Effect of nitrogen sources and vitamins on ligninolytic enzyme production by some white-rot fungi. Dye decolorization by selected culture filtrates. Bioresour. Technol. 101: 4554-4563.
    Pubmed CrossRef
  8. Shaul GM, Holdsworth TJ, Dempsey CR, Dostal KA. 1991. Fate of water soluble azo dyes in the activated sludge process. Chemosphere 22: 107-119.
    CrossRef
  9. Hongman H, Jiti Z, Jing W, Cuihong D, Bin Y. 2004. Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Process Biochem. 39: 1415-1419.
    CrossRef
  10. Li L, Wenkui D, Peng Y, Jian Z, Yinbo Q. 2009. Decolorisation of synthetic dyes by crude laccase from Rigidoporus lignosus W1. J. Chem. Technol. Biotechnol. 84: 399-404.
    CrossRef
  11. Ainsworth GC, Sparrow FK, Sussman AS. 1973. A taxonomic review with keys: basidiomycetes and lower fungi. In Ainsworth GC, Sparrow FK, Sussman AS (eds.). The Fungi, An Advanced Treatise, Vol. 4B. Academic Press, Orlando. USA.
  12. Lim SJ, Jeon SJ. 2014. Optimal conditions for laccase production from the white-rot fungus Marasmius scorodonius. Korean J. Microbiol. Biotechnol. 42: 225-231.
    CrossRef
  13. Schückel J, Matura A, van Pée KH. 2011. One-copper laccase-related enzyme from Marasmius sp.: purification, characterization and bleaching of textile dyes. Enzyme Microb. Technol. 48: 278-284.
    Pubmed CrossRef
  14. Perrella FW. 1988. EZ-FIT: a practical curve-fitting microcomputer program for the analysis of enzyme kinetic data on IBM-PC compatible computers. Anal. Biochem. 174:437-447.
    CrossRef
  15. Baldrian P. 2006. Fungal laccases – occurrence and properties. FEMS Microbiol. Rev. 30: 215-242.
    Pubmed CrossRef
  16. Liu H, Tong C, Du B, Liang S, Lin Y. 2015. Expression and characterization of LacMP, a novel fungal laccase of Moniliophthora perniciosa FA553. Biotechnol. Lett. 37: 1829-1835.
    Pubmed CrossRef
  17. Rheinhammar B. 1984. Laccase, pp. 4-10. In R. Lontie (ed.). Copper Proteins and Copper Enzymes. CRC Press, Inc., Boca Raton, FL. USA.
  18. Eggert C, Temp U, Eriksson KE. 1996. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus:purification and characterization of the laccase. Appl. Environ. Microbiol. 62: 1151-1158.
    Pubmed PMC
  19. Wood DA. 1980. Production, purification and properties of extracellular laccase of Agaricus bisporus. J. Gen. Microbiol. 177: 327-338.
    CrossRef
  20. De Vries OMH, Kooistra WHCF, Wessels JGH. 1986. Formation of an extracellular laccase by a Schizophyllum commune dikaryon. J. Gen. Microbiol. 132: 2817-2826.
    CrossRef
  21. Karhunen E, Niku-Paavola ML, Viikari L, Haltia T, van der Meer RA, Duine JA. 1990. A novel combination of prosthetic groups in a fungal laccase: PQQ and two copper atoms. FEBS Lett. 267: 6-8.
    CrossRef
  22. Okamoto K, Yanagi SO, Sakai T. 2000. Purification and characterization of extracellular laccase from Pleurotus ostreatus. Mycoscience 41: 7-13.
    CrossRef
  23. Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A, Sannia G. 1997. A n ovel white l accase f rom Pleurotus ostreatus. J. Biol. Chem. 271: 31301-31307.
    CrossRef
  24. Min KL, Kim YH, Kim YW, Jung HS, Hah YC. 2001. Characterization of a novel laccase produced by the woodrotting fungus Phellinus ribis. Arch. Biochem. Biophys. 392:279-286.
    Pubmed CrossRef
  25. Kaneko S, Cheng M, Murai H, Takenaka S, Murakami S, Aoki K. 2009. Purification and characterization of an extracellular laccase from Phlebia radiata strain BP-11-2 that decolorizes fungal melanin. Biosci. Biotechnol. Biochem. 73:939-942.
    Pubmed CrossRef
  26. Nakamura K, Go N. 2005. Function and molecular evolution of multicopper blue proteins. Cell. Mol. Life Sci. 62: 2050-2066.
    Pubmed CrossRef
  27. Robles A, Lucas R, Cienfuegos G, Gálvez A. 2000. Phenoloxidase (laccase) activity in strains of the hyphomycete Chalara paradoxa isolated from olive mill wastewater disposal ponds. Enzyme Microb. Technol. 26: 484-490.
    CrossRef
  28. Murugesan K, Kim YM, Jeon JR, Chang YS. 2009. Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum. J. Hazard. Mater. 168: 523-529.
    Pubmed CrossRef
  29. Mechichi T, Mhiri N, Sayadi S. 2006. Remazol Brilliant Blue R decolorization by the laccase from Trametes trogii. Chemosphere 64: 998-1005
    Pubmed CrossRef
  30. Khlifi R, Belbahri L, Woodward S, Ellouz M, Dhouib A, Sayadi S, Mechichi T. 2010. Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J. Hazard. Mater. 175: 802-808.
    Pubmed CrossRef
  31. El-Batal AI, ElKenawy NM, Yassin AS, Amin MA. 2015. Laccase production by Pleurotus ostreatus and i ts appl ication in synthesis of gold nanoparticles. Biotechnol. Rep. 5: 31-39.
    Pubmed PMC CrossRef
  32. Li J, McMillin DR. 1992. The removal of the type-2 copper from Rhus vernicifera laccase. Biochim. Biophys. Acta 28: 239-245.
    CrossRef
  33. D’Souza-Ticlo D, Sharma D, Raghukumar C. 2009. A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus. Mar. Biotechnol. (NY) 11: 725-737.
    Pubmed CrossRef
  34. Zheng Z, Li H, Li L, Shao W. 2012. Biobleaching of wheat straw pulp with recombinant laccase from the hyperthermophilic Thermus thermophiles. Biotechnol. Lett. 34: 541-547.
    Pubmed CrossRef
  35. Haibo Z, Yinglong Z, Feng H, Peiji G, Jiachuan C. 2009. Purification and characterization of a thermostable laccase with unique oxidative characteristics from Trametes hirsuta. Biotechnol. Lett. 31: 837-843.
    Pubmed CrossRef
  36. Reiss R, Ihssen J, Thöny-Meyer L. 2011. Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol. 11: 1-11.
    Pubmed PMC CrossRef
  37. Yang XQ, Zhao XX, Liu CY, Zheng Y, Qian SJ. 2009. Decolorization of azo, triphenylmethane and anthraquinone dyes by a newly isolated Trametes sp. SQ01 and its laccase. Process Biochem. 44: 1185-1189.
    CrossRef
  38. Grassi E, Scodeller P, Filiel N, Carballo R, Levin L. 2011. Potential of Trametes trogii c ul ture f l uids a nd i ts p urified laccase for the decolorization of different types of recalcitrant dyes without the addition of redox mediators. Int. Biodeterior. Biodegradation 65: 635-643.
    CrossRef
  39. Zouari-Mechichi H, Mechichi T, Dhouib A, Sayadi S, Martínez AT, Martínez MJ. 2006. Laccase purification and characterization from Trametes trogii isolated in Tunisia:decolorization of textile dyes by the purified enzyme. Enzyme Microb. Technol. 39: 141-148.
    CrossRef
  40. Soares GM, de Amorim MT, Costa-Ferreira M. 2001. Use of laccase together with redox mediators to decolourize remazol brilliant blue R. J. Biotechnol. 89: 123-129.
    CrossRef
  41. Reyes P, Pickard MA, Vazquez-Duhalt R. 1999. Hydroxybenzotriazole increases the range of textile dyes decolorized by immobilized laccase. Biotechnol. Lett. 21: 875-880.
    CrossRef

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Article

Research article

J. Microbiol. Biotechnol. 2017; 27(6): 1120-1127

Published online June 28, 2017 https://doi.org/10.4014/jmb.1701.01004

Copyright © The Korean Society for Microbiology and Biotechnology.

Purification and Characterization of the Laccase Involved in Dye Decolorization by the White-Rot Fungus Marasmius scorodonius

Sung-Jong Jeon 1, 2* and Su-Jin Lim 2

1Biomedical Engineering & Biotechnology Major, Division of Applied Bioengineering,, 2Department of Smart-Biohealth, Dong-Eui University, Busan 47340, Republic of Korea

Received: January 5, 2017; Accepted: April 4, 2017

Abstract

Marasmius scorodonius secretes an extracellular laccase in potato dextrose broth, and this
enzyme was purified up to 206-fold using (NH4)2SO4 precipitation and a Hi-trap Q Sepharose
column. The molecular mass of the purified laccase was estimated to be ~67 kDa by SDSPAGE.
The UV/vis spectrum of the enzyme was nontypical for laccases, and metal content
analysis revealed that the enzyme contains 1 mole of Fe and Zn and 2 moles of Cu per mole of
protein. The optimal pH for the enzymatic activity was 3.4, 4.0, and 4.6 with 2,2’-azino-bis(3-
ethylbenzothazoline-6-sulfonate) (ABTS), guaiacol, and 2,6-dimethoxy phenol as the substrate,
respectively. The optimal temperature of the enzyme was 75°C with ABTS as the substrate.
The enzyme was stable in the presence of some metal ions such as Ca2+, Cu2+, Ni2+, Mg2+, Mn2+,
Ba2+, Co2+, and Zn2+ at a low concentration (1 mM), whereas Fe2+ completely inhibited the
enzymatic activity. The enzymatic reaction was strongly inhibited by metal chelators and thiol
compounds except for EDTA. This enzyme directly decolorized Congo red, Malachite green,
Crystal violet, and Methylene green dyes at various decolorization rates of 63–90%. In the
presence of 1-hydroxybenzotriazole as a redox mediator, the decolorization of Reactive orange
16 and Remazol brilliant blue R was also achieved.

Keywords: Laccase, Marasmius scorodonius, synthetic dyes, decolorization

References

  1. Hoegger PJ, Kilaru S, James TY, Thacker JR, Kües U. 2006. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J. 273:2308-2326.
    Pubmed CrossRef
  2. Rivera-Hoyos CM, Morales-Álvarez ED, Poutou-Piñales RA, Pedroza-Rodríjuez AM, Rodríguez-Vázquez R, DelgadoBoada JM. 2013. Fungal laccases. Fungal Biol. Rev. 27: 67-82.
    CrossRef
  3. Bajpai P. 1999. Application of enzymes in the pulp and paper industry. Biotechnol. Prog. 15: 147-157.
    Pubmed CrossRef
  4. Durán N, Rosa MA, D’Annibale A, Gianfreda L. 2002. Applications of laccases and tyrosinases (phenoloxidases) immobilized on different supports: a review. Enzyme Microb. Technol. 31: 907-931.
    CrossRef
  5. Cameselle C, Pazos M, Lorenzo M, Sanromán MA. 2003. Enhanced decolourisation ability of laccase towards various synthetic dyes by an electrocatalysis technology. Biotechnol. Lett. 25: 603-606.
    Pubmed CrossRef
  6. Rim K, Lasssd B, Steve W, Mariem E, Abdelhafidh D, Sarni S, Tabar M. 2010. Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J. Hazard. Mater. 175: 802-808.
    Pubmed CrossRef
  7. Levin L, Melignani E, Ramos AM. 2010. Effect of nitrogen sources and vitamins on ligninolytic enzyme production by some white-rot fungi. Dye decolorization by selected culture filtrates. Bioresour. Technol. 101: 4554-4563.
    Pubmed CrossRef
  8. Shaul GM, Holdsworth TJ, Dempsey CR, Dostal KA. 1991. Fate of water soluble azo dyes in the activated sludge process. Chemosphere 22: 107-119.
    CrossRef
  9. Hongman H, Jiti Z, Jing W, Cuihong D, Bin Y. 2004. Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Process Biochem. 39: 1415-1419.
    CrossRef
  10. Li L, Wenkui D, Peng Y, Jian Z, Yinbo Q. 2009. Decolorisation of synthetic dyes by crude laccase from Rigidoporus lignosus W1. J. Chem. Technol. Biotechnol. 84: 399-404.
    CrossRef
  11. Ainsworth GC, Sparrow FK, Sussman AS. 1973. A taxonomic review with keys: basidiomycetes and lower fungi. In Ainsworth GC, Sparrow FK, Sussman AS (eds.). The Fungi, An Advanced Treatise, Vol. 4B. Academic Press, Orlando. USA.
  12. Lim SJ, Jeon SJ. 2014. Optimal conditions for laccase production from the white-rot fungus Marasmius scorodonius. Korean J. Microbiol. Biotechnol. 42: 225-231.
    CrossRef
  13. Schückel J, Matura A, van Pée KH. 2011. One-copper laccase-related enzyme from Marasmius sp.: purification, characterization and bleaching of textile dyes. Enzyme Microb. Technol. 48: 278-284.
    Pubmed CrossRef
  14. Perrella FW. 1988. EZ-FIT: a practical curve-fitting microcomputer program for the analysis of enzyme kinetic data on IBM-PC compatible computers. Anal. Biochem. 174:437-447.
    CrossRef
  15. Baldrian P. 2006. Fungal laccases – occurrence and properties. FEMS Microbiol. Rev. 30: 215-242.
    Pubmed CrossRef
  16. Liu H, Tong C, Du B, Liang S, Lin Y. 2015. Expression and characterization of LacMP, a novel fungal laccase of Moniliophthora perniciosa FA553. Biotechnol. Lett. 37: 1829-1835.
    Pubmed CrossRef
  17. Rheinhammar B. 1984. Laccase, pp. 4-10. In R. Lontie (ed.). Copper Proteins and Copper Enzymes. CRC Press, Inc., Boca Raton, FL. USA.
  18. Eggert C, Temp U, Eriksson KE. 1996. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus:purification and characterization of the laccase. Appl. Environ. Microbiol. 62: 1151-1158.
    Pubmed KoreaMed
  19. Wood DA. 1980. Production, purification and properties of extracellular laccase of Agaricus bisporus. J. Gen. Microbiol. 177: 327-338.
    CrossRef
  20. De Vries OMH, Kooistra WHCF, Wessels JGH. 1986. Formation of an extracellular laccase by a Schizophyllum commune dikaryon. J. Gen. Microbiol. 132: 2817-2826.
    CrossRef
  21. Karhunen E, Niku-Paavola ML, Viikari L, Haltia T, van der Meer RA, Duine JA. 1990. A novel combination of prosthetic groups in a fungal laccase: PQQ and two copper atoms. FEBS Lett. 267: 6-8.
    CrossRef
  22. Okamoto K, Yanagi SO, Sakai T. 2000. Purification and characterization of extracellular laccase from Pleurotus ostreatus. Mycoscience 41: 7-13.
    CrossRef
  23. Palmieri G, Giardina P, Bianco C, Scaloni A, Capasso A, Sannia G. 1997. A n ovel white l accase f rom Pleurotus ostreatus. J. Biol. Chem. 271: 31301-31307.
    CrossRef
  24. Min KL, Kim YH, Kim YW, Jung HS, Hah YC. 2001. Characterization of a novel laccase produced by the woodrotting fungus Phellinus ribis. Arch. Biochem. Biophys. 392:279-286.
    Pubmed CrossRef
  25. Kaneko S, Cheng M, Murai H, Takenaka S, Murakami S, Aoki K. 2009. Purification and characterization of an extracellular laccase from Phlebia radiata strain BP-11-2 that decolorizes fungal melanin. Biosci. Biotechnol. Biochem. 73:939-942.
    Pubmed CrossRef
  26. Nakamura K, Go N. 2005. Function and molecular evolution of multicopper blue proteins. Cell. Mol. Life Sci. 62: 2050-2066.
    Pubmed CrossRef
  27. Robles A, Lucas R, Cienfuegos G, Gálvez A. 2000. Phenoloxidase (laccase) activity in strains of the hyphomycete Chalara paradoxa isolated from olive mill wastewater disposal ponds. Enzyme Microb. Technol. 26: 484-490.
    CrossRef
  28. Murugesan K, Kim YM, Jeon JR, Chang YS. 2009. Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum. J. Hazard. Mater. 168: 523-529.
    Pubmed CrossRef
  29. Mechichi T, Mhiri N, Sayadi S. 2006. Remazol Brilliant Blue R decolorization by the laccase from Trametes trogii. Chemosphere 64: 998-1005
    Pubmed CrossRef
  30. Khlifi R, Belbahri L, Woodward S, Ellouz M, Dhouib A, Sayadi S, Mechichi T. 2010. Decolourization and detoxification of textile industry wastewater by the laccase-mediator system. J. Hazard. Mater. 175: 802-808.
    Pubmed CrossRef
  31. El-Batal AI, ElKenawy NM, Yassin AS, Amin MA. 2015. Laccase production by Pleurotus ostreatus and i ts appl ication in synthesis of gold nanoparticles. Biotechnol. Rep. 5: 31-39.
    Pubmed KoreaMed CrossRef
  32. Li J, McMillin DR. 1992. The removal of the type-2 copper from Rhus vernicifera laccase. Biochim. Biophys. Acta 28: 239-245.
    CrossRef
  33. D’Souza-Ticlo D, Sharma D, Raghukumar C. 2009. A thermostable metal-tolerant laccase with bioremediation potential from a marine-derived fungus. Mar. Biotechnol. (NY) 11: 725-737.
    Pubmed CrossRef
  34. Zheng Z, Li H, Li L, Shao W. 2012. Biobleaching of wheat straw pulp with recombinant laccase from the hyperthermophilic Thermus thermophiles. Biotechnol. Lett. 34: 541-547.
    Pubmed CrossRef
  35. Haibo Z, Yinglong Z, Feng H, Peiji G, Jiachuan C. 2009. Purification and characterization of a thermostable laccase with unique oxidative characteristics from Trametes hirsuta. Biotechnol. Lett. 31: 837-843.
    Pubmed CrossRef
  36. Reiss R, Ihssen J, Thöny-Meyer L. 2011. Bacillus pumilus laccase: a heat stable enzyme with a wide substrate spectrum. BMC Biotechnol. 11: 1-11.
    Pubmed KoreaMed CrossRef
  37. Yang XQ, Zhao XX, Liu CY, Zheng Y, Qian SJ. 2009. Decolorization of azo, triphenylmethane and anthraquinone dyes by a newly isolated Trametes sp. SQ01 and its laccase. Process Biochem. 44: 1185-1189.
    CrossRef
  38. Grassi E, Scodeller P, Filiel N, Carballo R, Levin L. 2011. Potential of Trametes trogii c ul ture f l uids a nd i ts p urified laccase for the decolorization of different types of recalcitrant dyes without the addition of redox mediators. Int. Biodeterior. Biodegradation 65: 635-643.
    CrossRef
  39. Zouari-Mechichi H, Mechichi T, Dhouib A, Sayadi S, Martínez AT, Martínez MJ. 2006. Laccase purification and characterization from Trametes trogii isolated in Tunisia:decolorization of textile dyes by the purified enzyme. Enzyme Microb. Technol. 39: 141-148.
    CrossRef
  40. Soares GM, de Amorim MT, Costa-Ferreira M. 2001. Use of laccase together with redox mediators to decolourize remazol brilliant blue R. J. Biotechnol. 89: 123-129.
    CrossRef
  41. Reyes P, Pickard MA, Vazquez-Duhalt R. 1999. Hydroxybenzotriazole increases the range of textile dyes decolorized by immobilized laccase. Biotechnol. Lett. 21: 875-880.
    CrossRef