A chloride tolerant laccase from the plant pathogen ascomycete Botrytis aclada expressed at high levels in Pichia pastoris

Journal of Biotechnology

Volumn 157, Issue 2, 2012, Pages 304-314

  Kittl, Roman ^a   Mueangtoom, Kitti ^b,c   Gonaus, Christoph ^a   Khazaneh, Shima Tahvilda ^a   Sygmund, Christoph ^a   Haltrich, Dietmar ^a,c   Ludwig, Roland ^a,c  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b UTTARADIT RAJABHAT UNIVERSITY   (Thailand)

^c AUSTRIAN CENTRE OF INDUSTRIAL BIOTECHNOLOGY   (Austria)

Author keywords

Ascomycete; Botrytis aclada; Chloride inhibition; Heterologous expression; Laccase; Pichia pastoris

Indexed keywords

ASCOMYCETE; BOTRYTIS ACLADA; HETEROLOGOUS EXPRESSION; LACCASES; PICHIA PASTORIS;

AMINO ACIDS; FERMENTATION; INDUSTRIAL APPLICATIONS; IONS; PHENOLS; SUBSTRATES; YEAST;

CHLORINE COMPOUNDS;

AMINO ACID; BIOFUEL; CHLORIDE; CHLORIDE ION; LACCASE; PHENOL DERIVATIVE; RECOMBINANT PROTEIN;

ARTICLE; BIOCATALYSIS; BOTRYTIS; CONTROLLED STUDY; ENZYME METABOLISM; ENZYME STABILITY; ENZYME SUBSTRATE; FED BATCH FERMENTATION; GLYCATION; MICHAELIS CONSTANT; MOLECULAR WEIGHT; NONHUMAN; NUCLEOTIDE SEQUENCE; PH; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION;

BENZOTHIAZOLES; BOTRYTIS; CATALYSIS; CHLORIDES; ENZYME STABILITY; FERMENTATION; GENE EXPRESSION; HYDROGEN-ION CONCENTRATION; LACCASE; ORGANISMS, GENETICALLY MODIFIED; PICHIA; RECOMBINANT PROTEINS; SULFONIC ACIDS;

BOTRYTIS ACLADA; FUNGI; PICHIA PASTORIS;

EID: 84855708375     PISSN: 01681656     EISSN: 18734863     Source Type: Journal    
DOI: 10.1016/j.jbiotec.2011.11.021     Document Type: Article

References (64)

1. Abianova A.R., Chulkin A.M., Vavilova E.A., Fedorova T.V., Loginov D.S., Koroleva O.V., Benevolenskii S.V. A heterologous production of the Trametes hirsuta laccase in the fungus Penicillium canescens. Prikl. Biokhim. Mikrobiol. 2010, 46:342-347.
2. Andberg M., Hakulinen N., Auer S., Saloheimo M., Koivula A., Rouvinen J., Kruus K. Essential role of the C-terminus in Melanocarpus albomyces laccase for enzyme production, catalytic properties and structure. FEBS J. 2009, 276:6285-6300.
3. Baker C.J.O., White T.C. Expression of laccase I and IV genes from Trametes versicolor in Trichoderma reesei. ACS Symp. Ser. 2001, 413-425.
4. Baldrian P. Fungal laccases-occurrence and properties. FEMS Microbiol. Rev. 2006, 30:215-242.
5. Bendtsen J.D., Nielsen H., von Heijne G., Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340:783-795.
6. Berka R.M., Schneider P., Golightly E.J., Brown S.H., Madden M., Brown K.M., Halkier T., Mondorf K., Xu F. Characterization of the gene encoding an extracellular laccase of Myceliophthora thermophila and analysis of the recombinant enzyme expressed in Aspergillus oryzae. Appl. Environ. Microbiol. 1997, 63:3151-3157.
7. Beyl Y., Guschin D.A., Shleev S., Schuhmann W. A chloride resistant high potential oxygen reducing biocathode based on a fungal laccase incorporated into an optimized Os-complex modified redox hydrogel. Electrochem. Commun. 2011, 13:474-476.
8. Bleve G., Lezzi C., Mita G., Rampino P., Perrotta C., Villanova L., Grieco F. Molecular cloning and heterologous expression of a laccase gene from Pleurotus eryngii in free and immobilized Saccharomyces cerevisiae cells. Appl. Microbiol. Biotechnol. 2008, 79:731-741.
9. Bohlin C., Jönsson L.J., Roth R., Van Zyl W.H. Heterologous expression of Trametes versicolor laccase in Pichia pastoris and Aspergillus niger. Appl. Biochem. Biotechnol. 2006, 129:195-214.
10. Brissos V., Pereira L., Munteanu F.D., Cavaco-Paulo A., Martins L.O. Expression system of CotA-laccase for directed evolution and high-throughput screenings for the oxidation of high-redox potential dyes. Biotechnol. J. 2009, 4:558-563.
11. 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.
12. Colao M.C., Lupino S., Garzillo A.M., Buonocore V., Ruzzi M. Heterologous expression of lcc1 gene from Trametes trogii in Pichia pastoris and characterization of the recombinant enzyme. Microb. Cell Fact. 2006, 5.
13. Cregg J.M., Russell K.A. Pichia protocols. Methods in Molecular Biology 1998, Humana Press, Totowa, NJ. D.R. Higgins, J.M. Cregg (Eds.).
14. Das N., Chakraborty T.K., Mukherjee M. Purification and characterization of a growth-regulating laccase from Pleurotus florida. J. Basic Microbiol. 2001, 41:261-267.
15. do Rosário Freixo M., Karmali A., Frazão C., Arteiro J.M. Production of laccase and xylanase from Coriolus versicolor grown on tomato pomace and their chromatographic behaviour on immobilized metal chelates. Process Biochem. 2008, 43:1265-1274.
16. Dubernet M., Ribereau-Gayon P., Lerner H.R., Harel E., Mayer A.M. Purification and properties of laccase from Botrytis cinerea. Phytochemistry 1977, 16:191-193.
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. Garzillo A.M.V., Colao M.C., Caruso C., Caporale C., Celletti D., Buonocore V. Laccase from the white-rot fungus Trametes trogii. Appl. Microbiol. Biotechnol. 1998, 49:545-551.
19. Guo M., Lu F., Du L., Pu J., Bai D. Optimization of the expression of a laccase gene from Trametes versicolor in Pichia methanolica. Appl. Microbiol. Biotechnol. 2006, 71:848-852.
20. Hakulinen N., Andberg M., Kallio J., Koivula A., Kruus K., Rouvinen J. A near atomic resolution structure of a Melanocarpus albomyces laccase. J. Struct. Biol. 2008, 162:29-39.
21. Hoegger P.J., Kilaru S., James T.Y., Thacker J.R., Kües U. Phylogenetic comparison and classification of laccase and related multicopper oxidase protein sequences. FEBS J. 2006, 273:2308-2326.
22. Hong F., Meinander N.Q., Jönsson L.J. Fermentation strategies for improved heterologous expression of laccase in Pichia pastoris. Biotechnol. Bioeng. 2002, 79:438-449.
23. Hong Y., Xiao Y., Zhou H., Fang W., Zhang M., Wang J., Wu L., Yu Z. Expression of a laccase cDNA from Trametes sp. AH28-2 in Pichia pastoris and mutagenesis of transformants by nitrogen ion implantation. FEMS Microbiol. Lett. 2006, 258:96-101.
24. 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.
25. Jaouani A., Guillén F., Penninckx M.J., Martínez A.T., Martínez M.J. Role of Pycnoporus coccineus laccase in the degradation of aromatic compounds in olive oil mill wastewater. Enzyme Microb. Technol. 2005, 36:478-486.
26. Kellner H., Luis P., Buscot F. Diversity of laccase-like multicopper oxidase genes in Morchellaceae: identification of genes potentially involved in extracellular activities related to plant litter decay. FEMS Microbiol. Ecol. 2007, 61:153-163.
27. Kiiskinen L.L., Saloheimo M. Molecular cloning and expression in Saccharomyces cerevisiae of Laccase gene from the ascomycete Melanocarpus albomyces. Appl. Environ. Microbiol. 2004, 70:137-144.
28. Kiiskinen L.L., Viikari L., Kruus K. Purification and characterisation of a novel laccase from the ascomycete Melanocarpus albomyces. Appl. Microbiol. Biotechnol. 2002, 59:198-204.
29. Kim J.M., Park S.M., Kim D.H. Heterologous expression of a tannic acid-inducible laccase3 of Cryphonectria parasitica in Saccharomyces cerevisiae. BMC Biotechnol. 2010, 10.
30. Kunamneni A., Ghazi I., Camarero S., Ballesteros A., Plou F.J., Alcalde M. Decolorization of synthetic dyes by laccase immobilized on epoxy-activated carriers. Process Biochem. 2008, 43:169-178.
31. Leitner C., Hess J., Galhaup C., Ludwig R., Nidetzky B., Kulbe K., Haltrich D. Purification and characterization of a laccase from the white-rot fungus Trametes multicolor. Appl. Biochem. Biotechnol. 2002, 98-100:497-507.
32. Li J.F., Hong Y.Z., Xiao Y.Z., Xu Y.H., Fang W. High production of laccase B from Trametes sp. in Pichia pastoris. World J. Microbiol. Biotechnol. 2007, 23:741-745.
33. Li K., Xu F., Eriksson K.E.L. Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl. Environ. Microbiol. 1999, 65:2654-2660.
34. Liu W., Chao Y., Liu S., Bao H., Qian S. Molecular cloning and characterization of a laccase gene from the basidiomycete Fome lignosus and expression in Pichia pastoris. Appl. Microbiol. Biotechnol. 2003, 63:174-181.
35. Luis P., Walther G., Kellner H., Martin F., Buscot F. Diversity of laccase genes from basidiomycetes in a forest soil. Soil Biol. Biochem. 2004, 36:1025-1036.
36. Madzak C., Otterbein L., Chamkha M., Moukha S., Asther M., Gaillardin C., Beckerich J.M. Heterologous production of a laccase from the basidiomycete Pycnoporus cinnabarinus in the dimorphic yeast Yarrowia lipolytica. FEMS Yeast Res. 2005, 5:635-646.
37. Maté D., García-Burgos C., García-Ruiz E., Ballesteros A.O., Camarero S., Alcalde M. Laboratory evolution of high-redox potential laccases. Chem. Biol. 2010, 17:1030-1041.
38. Mayer A.M., Staples R.C. Laccase: new functions for an old enzyme. Phytochemistry 2002, 60:551-565.
39. Mueangtoom K., Kittl R., Mann O., Haltrich D., Ludwig R. Low pH dye decolorization with ascomycete Lamprospora wrightii laccase. Biotechnol. J. 2010, 5:857-870.
40. Niladevi K.N., Jacob N., Prema P. Evidence for a halotolerant-alkaline laccase in Streptomyces psammoticus: purification and characterization. Process Biochem. 2008, 43:654-660.
41. 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.
42. Piscitelli A., Giardina P., Mazzoni C., Sannia G. Recombinant expression of Pleurotus ostreatus laccases in Kluyveromyces lactis and Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 2005, 69:428-439.
43. 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.
44. Riva S. Laccases: blue enzymes for green chemistry. Trends Biotechnol. 2006, 24:219-226.
45. Robles A., Lucas R., Martínez-Cañamero M., Ben Omar N., Pérez R., Gálvez A. Characterisation of laccase activity produced by the hyphomycete Chalara (syn. Thielaviopsis) paradoxa CH32. Enzyme Microb. Technol. 2002, 31:516-522.
46. Rodgers C.J., Blanford C.F., Giddens S.R., Skamnioti P., Armstrong F.A., Gurr S.J. Designer laccases: a vogue for high-potential fungal enzymes?. Trends Biotechnol. 2010, 28:63-72.
47. Ruijssenaars H.J., Hartmans S. A cloned Bacillus halodurans multicopper oxidase exhibiting alkaline laccase activity. Appl. Microbiol. Biotechnol. 2004, 65:177-182.
48. Ryan S., Schnitzhofer W., Tzanov T., Cavaco-Paulo A., Gübitz G.M. An acid-stable laccase from Sclerotium rolfsii with potential for wool dye decolourization. Enzyme Microb. Technol. 2003, 33:766-774.
49. Saloheimo M., Niku-Paavola M.L. Heterologous production of a ligninolytic enzyme: expression of the Phlebia radiata laccase gene in Trichoderma reesei. Nat. Biotechnol. 1991, 9:987-990.
50. Santhanam N., Vivanco J.M., Decker S.R., Reardon K.F. Expression of industrially relevant laccases: prokaryotic style. Trends Biotechnol. 2011, 29:480-489.
51. Shleev S., Nikitina O., Christenson A., Reimann C.T., Yaropolov A.I., Ruzgas T., Gorton L. Characterization of two new multiforms of Trametes pubescens laccase. Bioorg. Chem. 2007, 35:35-49.
52. Slomczynski D., Nakas J.P., Tanenbaum S.W. Production and characterization of laccase from Botrytis cinerea 61-34. Appl. Environ. Microbiol. 1995, 61:907-912.
53. 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.
54. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol. Biol. Evol. 2011, 10.1093/molbev/msr121.
55. Trovaslet M., Enaud E., Guiavarc'h Y., Corbisier A.M., Vanhulle S. Potential of a Pycnoporus sanguineus laccase in bioremediation of wastewater and kinetic activation in the presence of an anthraquinonic acid dye. Enzyme Microb. Technol. 2007, 41:368-376.
56. Ullrich R., Le M.H., Nguyen L.D., Hofrichter M. Laccase from the medicinal mushroom Agaricus blazei: production, purification and characterization. Appl. Microbiol. Biotechnol. 2005, 67:357-363.
57. 2O with high-operational stability and resistance to chloride inhibition. Biosens. Bioelectron. 2008, 24:531-537.
58. Whelan S., Goldman N. A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol. Biol. Evol. 2001, 18:691-699.
59. Xu F. Oxidation of phenols, anilines, and benzenethiols by fungal laccases: correlation between activity and redox potentials as well as halide inhibition. Biochemistry 1996, 35:7608-7614.
60. Xu F., Berka R.M., Wahleithner J.A., Nelson B.A., Shuster J.R., Brown S.H., Palmer A.E., Solomon E.I. Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem. J. 1998, 334:63-70.
61. Yaver D.S., Overjero M.D.C., Xu F., Nelson B.A., Brown K.M., Halkier T., Bernauer S., Brown S.H., Kauppinen S. Molecular characterization of laccase genes from the basidiomycete Coprinus cinereus and heterologous expression of the laccase Lcc1. Appl. Environ. Microbiol. 1999, 65:4943-4948.
62. Yaver D.S., Xu F., Golightly E.J., Brown K.M., Brown S.H., Rey M.W., Schneider P., Halkier T., Mondorf K., Dalbøge H. Purification, characterization, molecular cloning, and expression of two laccase genes from the white rot basidiomycete Trametes villosa. Appl. Environ. Microbiol. 1996, 62:834-841.
63. Zhou H.M., Hong Y.Z., Xiao Y.Z., Cui T.J., Wang X.T., Pu C.L. High output of a Trametes laccase in Pichia pastoris and characterization of recombinant enzymes. Chin. J. Biotechnol. 2007, 23:1055-1059.
64. Zouari N., Romette J.L., Thomas D. Purification and properties of two laccase isoenzymes produced by Botrytis cinerea. Appl. Biochem. Biotechnol. 1987, 15:213-225.