Decolorization of different dyes by a newly isolated white-rot fungi strain Ganoderma sp.En3 and cloning and functional analysis of its laccase gene

Journal of Hazardous Materials

Volumn 192, Issue 2, 2011, Pages 855-873

  Zhuo, Rui ^a,b   Ma, Li ^a   Fan, Fangfang ^a,b   Gong, Yangmin ^b   Wan, Xia ^b   Jiang, Mulan ^b   Zhang, Xiaoyu ^a   Yang, Yang ^a,b  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

Cis acting elements; Decolorization of dyes; Ganoderma sp.En3; Laccase gene; White rot fungi

Indexed keywords

CIS-ACTING ELEMENT; DECOLORIZATION OF DYES; GANODERMA; LACCASE GENE; WHITE ROT FUNGI;

CLONING; TEXTILE PROCESSING; TEXTILES; YEAST;

GENE ENCODING;

COMPLEMENTARY DNA; COPPER; DYE; LACCASE;

BIODEGRADATION; DYE; EFFLUENT; ENZYME ACTIVITY; GENE EXPRESSION; MOLECULAR ANALYSIS; MUSHROOM; PHYTOTOXICITY; PROTEIN; RECOMBINATION; RICE; TEXTILE INDUSTRY;

AMINO ACID SEQUENCE; ARTICLE; CHINA; CLONING; CODON; CONTROLLED STUDY; DECOLORIZATION; DETOXIFICATION; DNA FLANKING REGION; EFFLUENT; FUNGAL STRAIN; FUNGUS ISOLATION; GANODERMA; GENE; GENE EXPRESSION; GENETIC CODE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYTOTOXICITY; PICHIA PASTORIS; PROMOTER REGION; PROTEIN BINDING; RICE; WHEAT; WHITE ROT FUNGUS;

BASE SEQUENCE; CLONING, MOLECULAR; COLOR; COLORING AGENTS; DNA PRIMERS; GANODERMA; LACCASE;

CHINA;

FUNGI; GANODERMA; ORYZA SATIVA; PICHIA PASTORIS; TRITICUM AESTIVUM;

EID: 79960160653     PISSN: 03043894     EISSN: 18733336     Source Type: Journal    
DOI: 10.1016/j.jhazmat.2011.05.106     Document Type: Article

References (74)

1. Thurston C.F. The structure and function of fungal laccases. Microbiology 1994, 140:19-26.
2. Baldrian P. Laccases-occurrence and properties. FEMS Microbiol. Rev. 2006, 30:215-242.
3. Eggert C., Temp U., Eriksson K.E.L. Laccase is essential for lignin degradation by the white-rot fungus Pycnoporus cinnabarinus. FEBS Lett. 1997, 407:89-92.
4. Zhao J., Kwan H.S. Characterization, molecular cloning, and differential expression analysis of laccase genes from the edible mushroom Lentinula edodes. Appl. Environ. Microbiol. 1999, 65:4908-4913.
5. Suguimoto H.H., Barbosa A.M., Dekker R.F.H., Castro-Gomez R.J.H. Veratryl alcohol stimulates fruiting body formation in the oyster mushroom, Pleurotus ostreatus. FEMS Microbiol. Lett. 2001, 194:235-238.
6. Chen S.C., Ge W., Buswell J.A. Molecular cloning of a new laccase from the edible straw mushroom Volvariella volvacea: possible involvement in fruit body development. FEMS Microbiol. Lett. 2004, 230:171-176.
7. Choi G.H., Larson T.G., Nuss D.L. Molecular analysis of the laccase gene from the chestnut blight fungus and selective suppression of its expression in an isogenic hypovirulent strain. Mol. Plant Microbe Interact. 1992, 5:119-128.
8. Williamson P.R., Wakamatsu K., Ito S. Melanin biosynthesis in Cryptococcus neoformans. J. Bacteriol. 1998, 180:1570-1572.
9. Nagai M., Kawata M., Watanabe H., Ogawa M., Saito K., Takesawa T., Kanda K., Sato T. Important role of fungal intracellular laccase for melanin synthesis, purification and characterization of an intracellular laccase from Lentinula edodes fruit bodies. Microbiology 2003, 149:2455-2462.
10. Shuttleworth K., Bollag J.M. Soluble and immobilized laccase as catalysts for the transformation of substituted phenols. Enzyme Microb. Technol. 1986, 8:171-177.
11. Yaropolov A.I., Skorobogat'ko O.V., Vartanov S.S., Varfolomeyev S.D. Laccase: properties, catalytic mechanism, and applicability. Appl. Biochem. Biotechnol. 1994, 49:257-280.
12. Duran N., Esposito E. Potential applications of oxidative enzymes and phenoloxidase-like compounds in wastewater and soil treatment, a review. Appl. Catal. B: Environ. 2000, 28:83-99.
13. Mayer A.M., Staples R.C. Laccase, new functions for an old enzyme. Phytochemistry 2002, 60:551-565.
14. Jönsson L.J., Sjöström K., Häggström I., Nyman P.O. Characterization of a laccase gene from the white rot fungus Trametes versicolor and structural features of basdiomycete laccases. Biochim. Biophys. Acta 1995, 1251:210-215.
15. Yaver D.S., Xu F., Golightly E.J., Brown K.M., Brown S.H., Rey M.W., Schneider P., Halkier T., Mondorf K., Dalboge H. Purification, characterization, molecular cloning and expression of two laccase genes from the white rot basidimoycete Trametes villosa. Appl. Environ. Microbiol. 1996, 62:834-841.
16. Ong E., Brent W., Pollock R., Smith M. Cloning and sequence analysis of two laccase complementary DNAs from the ligninolytic basidiomycete Trametes versicolor. Gene 1997, 196:113-119.
17. Galhaup C., Goller S., Peterbauer C.K., Strauss J., Haltrich D. Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology 2002, 148:2159-2169.
18. Pezzella C., Autore F., Giardina P., Piscitelli A., Sannia G., Faraco V. The Pleurotus ostreatus laccase multi-gene family, isolation and heterologous expression of new family members. Curr. Genet. 2009, 55:45-57.
19. Otterbein L., Record E., Longhi S., Asther M., Moukha S. Molecular cloning of the cDNA encoding laccase from Pycnoporus cinnabarinus I-937 and expression in Pichia pastoris. Eur. J. Biochem. 2000, 267:1619-1625.
20. Soden D.M., O'Callaghan J., Dobson A.D.W. Molecular cloning of a laccase isozyme gene from Pleurotus sajor-caju and expression in the heterologous Pichia pastoris host. Microbiology 2002, 148:4003-4014.
21. Guo M., Lu F.P., Pu J., Bai D.Q., Du L.X. Molecular cloning of the cDNA encoding laccase from Trametes versicolor and heterologous expression in Pichia methanolica. Appl. Microbiol. Biotechnol. 2005, 69:178-183.
22. Cassland P., Jönsson L.J. Characterization of a gene encoding Trametes versicolor laccase A and improved heterologous expression in Saccharomyces cerevisiae by decreased cultivation temperature. Appl. Microbiol. Biotechnol. 1999, 52:393-400.
23. Hoshida H., Nakao M., Kanazawa H., Kubo K., Hakukawa T., Morimasa K., Akada R., Nishizawa Y. Isolation of five laccase gene sequences from the white-rot fungus Trametes sanguinea by PCR, and cloning, characterization and expression of the laccase cDNA in yeasts. J. Biosci. Bioeng. 2001, 92:372-380.
24. Bulter T., Alcalde M., Sieber V., Meinhold P., Schlachtbauer C., Arnold F.H. Functional expression of a fungal laccase in Saccharomyces cerevisiae by directed evolution. Appl. Environ. Microbiol. 2003, 69:987-995.
25. Faraco V., Ercole C., Festa G., Giardina P., Piscitelli A., Sannia G. Heterologous expression of heterodimeric laccases from Pleurotus ostreatus in Kluyveromyces lactis. Appl. Microbiol. Biotechnol. 2008, 77:1329-1335.
26. Jolivalt C., Madzak C., Brault A., Caminade E., Malosse C., Mougin C. Expression of laccase IIIb from the white-rot fungus Trametes versicolor in the yeast Yarrowia lipolytica for environmental applications. Appl. Microbiol. Biotechnol. 2005, 66:450-456.
27. Larrondo L.F., Avila M., Salas L., Cullen D., Vicuna R. Heterologous expression of laccase cDNA from Ceriporiopsis subvermispora yields copper-activated apoprotein and complex isoform patterns. Microbiology 2003, 149:1177-1182.
28. Record E., Punt P.J., Chamkha M., Labat M., van Den Hondel C.A.M.J.J., Asther M. Expression of the Pycnoporus cinnabarinus laccase gene in Aspergillus niger and characterization of the recombinant enzyme. Eur. J. Biochem. 2002, 269:602-609.
29. Hoshida H., Fujita T., Murata K., Kubo K., Akada R. Copper-dependent production of a Pycnoporus coccineus extracellular laccase in Aspergillus oryzae and Saccharomyces cerevisiae. Biosci. Biotechnol. Biochem. 2005, 69:1090-1097.
30. Saloheimo M., Niku-Paavola M.L. Heterologous production of a ligninolytic enzyme: expression of the Phlebia radiata laccase gene in Trichoderma reesei. Biotechnology 1991, 9:987-990.
31. Kiiskinen L.L., Kruus K., Bailey M., Ylosmaki E., Siika-aho M., Saloheimo M. Expression of Melanocarpus albomyces laccase in Trichoderma reesei and characterization of the purified enzyme. Microbiology 2004, 150:3065-3074.
32. Collins P.J., Dobson A.D.W. Regulation of laccase gene transcription in Trametes versicolor. Appl. Environ. Microbiol. 1997, 63:3444-3450.
33. Soden D.M., Dobson A.D.W. Differential regulation of laccase gene expression in Pleurotus sajor-caju. Microbiology 2001, 147:1755-1763.
34. Mansur M., Suarez T., Gonzalez A.E. Differential expression in the laccase gene family from basidiomycete I-62 (CECT 20197). Appl. Environ. Microbiol. 1998, 64:771-774.
35. Terrón M.C., González T., Carbajo J.M., Yagüe S., Arana-Cuenca A., Téllez A., Dobson A.D., González A.E. Structural close-related aromatic compounds have different effects on laccase activity and on lcc gene expression in the ligninolytic fungus Trametes sp. I-62. Fungal Genet. Biol. 2004, 41:954-962.
36. Liu Y.G., Mitsukawa N., Oosumi T., Whittier R.F. Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J. 1995, 8:457-463.
37. Wang S.M., He J., Cui Z.L., Li S.P. Self-formed adaptor PCR, a simple and efficient method for chromosome walking. Appl. Environ. Microbiol. 2007, 73:5048-5051.
38. Eggert C., Temp U., Eriksson K.E. The ligninolytic system of the white rot fungus Pycnoporus cinnabarinus, purification and characterization of the laccase. Appl. Environ. Microbiol. 1996, 62:1151-1158.
39. Palmieri G., Giardina P., Bianco C., Fontanella B., Sannia G. Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Appl. Environ. Microbiol. 2000, 66:920-924.
40. Revankar M.S., Lele S.S. Synthetic dye decolorization by white rot fungus, Ganoderma sp. WR-1. Bioresour. Technol. 2007, 98:775-780.
41. Steffen K.T., Hofrichter M., Hatakka A. Mineralisation of 14C-labelled synthetic lignin and ligninolytic enzyme activities of litter-decomposing basidiomycetous fungi. Appl. Microbiol. Biotechnol. 2000, 54:819-825.
42. Archibald F.S. A new assay for lignin-type peroxidases employing the dye Azure B. Appl. Environ. Microbiol. 1992, 58:3110-3116.
43. Jadhav J.P., Govindwar S.P. Biotransformation of malachite green by Saccharomyces cerevisiae MTCC 463. Yeast 2006, 23:315-323.
44. Makas Y.G., Kalkan N.A., Aksoy S., Altinok H., Hasirci N. Immobilization of laccase in k-carrageenan based semi-interpenetrating polymer networks. J. Biotechnol. 2010, 148:216-220.
45. Vijayaraghavan K., Lee M.W., Yun Y.S. A new approach to study the decolorization of complex reactive dye bath effluent by biosorption technique. Bioresour. Technol. 2008, 99:5778-5785.
46. Murugesan K., Kim Y.M., Jeon J.R., Chang Y.S. Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum. J. Hazard. Mater. 2009, 168:523-529.
47. Mohorcic M., Teodorovic S., Golob V., Friedrich J. Fungal and enzymatic decolourisation of artificial textile dye baths. Chemosphere 2006, 63:1709-1717.
48. Osma J.F., Toca-Herrera J.L., Rodriguez-Couto S. Biodegradation of a simulated textile effluent by immobilised-coated laccase in laboratory-scale reactors. Appl. Catal. A: Gen. 2010, 373:147-153.
49. Parshetti G., Kalme S., Saratale G., Govindwar S. Biodegradation of Malachite green by Kocuria rosea MTCC 1532. Acta Chim. Slov. 2006, 53:492-498.
50. Liu W.X., Chao Y.P., Yang X.Q., Bao H.B., Qian S.J. Biodecolorization of azo, anthraquinonic and triphenylmethane dyes by white-rot fungi and a laccase-secreting engineered strain. J. Ind. Microbiol. Biotechnol. 2004, 31:127-132.
51. Ayed L., Chaieb K., Cheref A., Bakhrouf A. Biodegradation of triphenylmethane dye malachite green by Sphingomonas paucimobilis. World J. Microbiol. Biotechnol. 2009, 25:705-711.
52. Nyanhongo G.S., Gomes J., Gübitz G.M., Zvauya R., Read J., Steiner W. Decolorization of textile dyes by laccases from a newly isolated strain of Trametes modesta. Water Res. 2002, 36:1449-1456.
53. D'Souza D.T., Tiwari R., Kumar Sah A., Raghukumar C. Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme Microb. Technol. 2006, 38:504-511.
54. Jadhav U.U., Dawkar V.V., Ghodake G.S., Govindwar S.P. Biodegradation of Direct Red 5B, a textile dye by newly isolated Comamonas sp. UVS. J. Hazard. Mater. 2008, 158:507-516.
55. Papinutti V.L., Forchiassin F. Modification of malachite green by Fomes sclerodermeus and reduction of toxicity to Phanerochaete chrysosporium. FEMS Microbiol. Lett. 2004, 231:205-209.
56. Knapp J.S., Newby P.S., Reece L.P. Decolorization of dyes by wood-rotting basidiomecete fungi. Enzyme Microb. Technol. 1995, 17:664-668.
57. Murao S., Hinode Y., Matsumura E., Numata A., Kawai K., Ohishi H., Jin H., Oyama H., Shin T. A novel laccase inhibitor, N-hydroxyglycine, produced by Penicillium citrinum YH-31. Biosci. Biotechnol. Biochem. 1992, 56:987-988.
58. Kim Y., Yeo S., Song H.G., Choi H.T. Enhanced expression of laccase during the degradation of endocrine disrupting chemicals in Trametes versicolor. J. Microbiol. 2008, 46:402-407.
59. Faraco V., Pezzella C., Miele A., Giardina P., Sannia G. Bio-remediation of colored industrial wastewaters by the white-rot fungi Phanerochaete chrysosporium and Pleurotus ostreatus and their enzymes. Biodegradation 2009, 20:209-220.
60. Verma A.K., Raghukumar C., Verma P., Shouche Y.S., Naik C.G. Four marine-derived fungi for bioremediation of raw textile mill effluents. Biodegradation 2010, 21:217-233.
61. Balan D.S.L., Monteiro R.T.R. Decolorization of textile indigo dye by ligninolytic fungi. J. Biotechnol. 2001, 89:141-145.
62. Spadaro J.T., Isabelle L., Renganathan V. Hydroxyl radical mediate degradation of azo dyes: evidence for benzene generation. Environ. Sci. Technol. 1994, 28:1389-1393.
63. Murugesan K., Yang I.H., Kim Y.M., Jeon J.R., Chang Y.S. Enhanced transformation of malachite green by laccase of Ganoderma lucidum in the presence of natural phenolic compounds. Appl. Microbiol. Biotechnol. 2009, 82:341-350.
64. Tong P.G., Hong Y.Z., Xiao Y.Z., Zhang M., Tu X.M., Cui T.G. High production of laccase by a new basidiomycete, Trametes sp. Biotechnol. Lett. 2007, 29:295-301.
65. Kulmberg P., Mathieu M., Dowzer C.E.A., Kelly J.M., Felenbok B. Specific binding sites in the alcR and alcA promoters of the ethanol regulon for the CreA repressor mediating carbon catabolite repression in Aspergillus nidulans. Mol. Microbiol. 1993, 7:847-857.
66. Strauss J., Horvath H.K., Abdallah B.M., Kindermann J., Mach R.L., Kubicek C.P. The function of CreA, the carbon catabolite repressor of Aspergillus nidulans, is regulated at the transcriptional and post-transcriptional level. Mol. Microbiol. 1999, 32:169-178.
67. Thiele D.J. Metal regulated transcription in eukaryotes. Nucleic Acids Res. 1992, 20:1183-1191.
68. Rushmore T.H., King R.G., Paulson K.E., Pickett C.B. Regulation of glutathione S-transferase Ya subunit gene expression, identification of a unique xenobiotic-responsive element controlling inducible expression by planar aromatic compounds. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:3826-3830.
69. Treger J.M., Magee T.R., McEntee K. Functional analysis of the stress response element and its role in the multistress response of Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 1998, 243:13-19.
70. Thiele D.J. ACE1 regulates expression of the Saccharomyces cerevisiae metallothionein gene. Mol. Cell. Biol. 1988, 8:2745-2752.
71. Thorvaldsen J.L., Sewell A.K., McGowen C.L., Winge D.R. Regulation of metallothionein genes by the ACE1 and AMT1 transcription factors. J. Biol. Chem. 1993, 268:12512-12518.
72. José M.Á., Paulo C., Rodrigo A.M., Rubén P., Paulina A.S., Rafael V. Expression of genes encoding laccase and manganese-dependent peroxidase in the fungus Ceriporiopsis subvermispora is mediated by an ACE1-like copper-fist transcription factor. Fungal Genet. Biol. 2009, 46:104-111.
73. Fu Y.H., Marzluf G.A. nit-2, the major positive-acting nitrogen regulatory gene of Neurospora crassa, encodes a sequence-specific DNA-binding protein. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:5331-5335.
74. Mager W.H., De Kruijff A.J. Stress-induced transcriptional activation. Microbiol. Rev. 1995, 59:506-531.