New colorimetric screening assays for the directed evolution of fungal laccases to improve the conversion of plant biomass

BMC Biotechnology

Volumn 13, Issue , 2013, Pages

  Pardo, Isabel ^a   Chanagá, Xiomara ^a   Vicente, Ana I ^a   Alcalde, Miguel ^b   Camarero, Susana ^a  

^a CENTRO DE INVESTIGACIONES BIOLÓGICAS   (Spain)

^b INSTITUTO DE CATÁLISIS Y PETROLEOQUÍMICA   (Spain)

Author keywords

Dyes; High throughput screening; Laccase; Lignocellulose; S type phenolic mediators; Violuric acid

Indexed keywords

HIGH-THROUGHPUT SCREENING; LACCASES; LIGNOCELLULOSE; S-TYPE PHENOLIC MEDIATORS; VIOLURIC ACID;

ASSAYS; AZO DYES; BIOCONVERSION; BIOMASS; CELLULOSE; COLOR; COLORIMETRY; DETOXIFICATION; DYEING; DYES; LIBRARIES; LIGNIN; OXIDATION; REDOX REACTIONS; SECONDARY BATTERIES; WOOLEN AND WORSTED YARN; YEAST;

ENZYMES;

ACETOSYRINGONE; BRILLIANT BLUE; EVANS BLUE; LACCASE; LIGNOCELLULOSE; METHYL ORANGE; PHENOL DERIVATIVE; SINAPIC ACID; SYRINGALDEHYDE; UNCLASSIFIED DRUG;

ARTICLE; BIOMASS CONVERSION; COLORIMETRY; CONTROLLED STUDY; DECOLORIZATION; ENZYME SUBSTRATE; HIGH THROUGHPUT SCREENING; LIMIT OF DETECTION; OXIDATION REDUCTION POTENTIAL; PEPTIDE LIBRARY; PROTEIN DEGRADATION; PROTEIN ENGINEERING; SACCHAROMYCES CEREVISIAE; SOLID;

SACCHAROMYCES CEREVISIAE;

AZO COMPOUNDS; BARBITURATES; BIOMASS; COLORIMETRY; CULTURE MEDIA; DIRECTED MOLECULAR EVOLUTION; EVANS BLUE; FUNGAL PROTEINS; HIGH-THROUGHPUT SCREENING ASSAYS; LACCASE; LIGNIN; OXIDATION-REDUCTION; PHENOL; PROTEIN ENGINEERING; REPRODUCIBILITY OF RESULTS; SACCHAROMYCES CEREVISIAE;

EID: 84886229698     PISSN: None     EISSN: 14726750     Source Type: Journal    
DOI: 10.1186/1472-6750-13-90     Document Type: Article

References (47)

1. Kunamneni A, Camarero S, Garcia-Burgos C, Plou FJ, Ballesteros A, Alcalde M. Engineering and applications of fungal laccases for organic synthesis. Microb Cell Fact 2008, 7:32. 10.1186/1475-2859-7-32, 2613868, 19019256.
2. Rodríguez-Couto S, Toca JL. Industrial and biotechnological applications of laccases: a review. Biotechnol Adv 2006, 24:500-513. 10.1016/j.biotechadv.2006.04.003, 16716556.
3. Shleev S, Persson P, Shumakovich G, Mazhugo Y, Yaropolov A, Ruzgas T, Gorton L. Laccase-based biosensors for monitoring lignin. Enzyme Microb Technol 2006, 39:835-840.
4. Xu F, Palmer AE, Yaver DS, Berka RM, Gambetta GA, Brown SH, Solomon EI. Targeted mutations in a Trametes villosa laccase - Axial perturbations of the T1 copper. J Biol Chem 1999, 274:12372-12375. 10.1074/jbc.274.18.12372, 10212209.
5. Camarero S, Galletti GC, Martínez AT. Preferential degradation of phenolic lignin-units by two white-rot fungi. Appl Environ Microbiol 1994, 60:4509-4516. 202012, 7811086.
6. Cañas A, Alcalde M, Plou FJ, Martínez MJ, Martínez AT, Camarero S. Transformation of polycyclic aromatic hydrocarbons by laccase is strongly enhanced by phenolic compounds present in soil. Environ Sci Technol 2007, 41:2964-2971. 10.1021/es062328j, 17533865.
7. Camarero S, Ibarra D, Martínez MJ, Martínez AT. Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 2005, 71:1775-1784. 10.1128/AEM.71.4.1775-1784.2005, 1082544, 15812000.
8. Nousiainen P, Maijala P, Hatakka A, Martínez AT, Sipila J. Syringyl-type simple plant phenolics as mediating oxidants in laccase catalyzed degradation of lignocellulosic materials: model compound studies. Holzforschung 2009, 63:699-704.
9. Torres-Duarte C, Roman R, Tinoco R, Vázquez-Duhalt R. Halogenated pesticide transformation by a laccase-mediator system. Chemosphere 2009, 77:687-692. 10.1016/j.chemosphere.2009.07.039, 19695672.
10. Cañas AI, Camarero S. Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 2010, 28:694-705. 10.1016/j.biotechadv.2010.05.002, 20471466.
11. Kikuzaki H, Hisamoto M, Hirose K, Akiyama K, Taniguchi H. Antioxidant properties of ferulic acid and its related compounds. J Agric Food Chem 2002, 50:2161-2168. 10.1021/jf011348w, 11902973.
12. Baker CJ, Mock NM, Whitaker BD, Roberts DP, Rice CP, Deahl KL, Aver'yanov AA. Involvement of acetosyringone in plant-pathogen recognition. Biochem Biophys Res Commun 2005, 328:130-136. 10.1016/j.bbrc.2004.12.153, 15670760.
13. Aracri E, Fillat A, Colom JF, Gutiérrez A, del Río JC, Martínez AT, Vidal T. Enzymatic grafting of simple phenols on flax and sisal pulp fibres using laccases. Bioresour Technol 2010, 101:8211-8216. 10.1016/j.biortech.2010.05.080, 20580550.
14. Wu GX, Heitz M, Chornet E. Improved alkaline oxidation process for the production of aldehydes (vanillin and syringaldehyde) from steam-explosion hardwood lignin. Ind Eng Chem Res 1994, 33:718-723.
15. Pinto PCR, da Silva EAB, Rodrigues AE. Insights into oxidative conversion of lignin to high-added-value phenolic aldehydes. Ind Eng Chem Res 2011, 50:741-748.
16. Camarero S, Ibarra D, Martínez AT, Romero J, Gutiérrez A, del Río JC. Paper pulp delignification using laccase and natural mediators. Enzyme Microb Technol 2007, 40:1264-1271.
17. Parawira W, Tekere M. Biotechnological strategies to overcome inhibitors in lignocellulose hydrolysates for ethanol production: review. Crit Rev Biotechnol 2011, 31:20-31. 10.3109/07388551003757816, 20513164.
18. Jurado M, Prieto A, Martínez-Alcalá MA, Martínez AT, Martínez MJ. Laccase detoxification of steam-exploded wheat straw for second generation bioethanol. Bioresour Technol 2009, 100:6378-6384. 10.1016/j.biortech.2009.07.049, 19683434.
19. Alvira P, Moreno AD, Ibarra D, Sáez F, Ballesteros M. Improving the fermentation performance of saccharomyces cerevisiae by laccase during ethanol production from steam-exploded wheat straw at high-substrate loadings. Biotechnol Prog 2013, 29:74-82. 10.1002/btpr.1666, 23143932.
20. Arnold FH, Volkov AA. Directed evolution of biocatalysts. Curr Opin Chem Biol 1999, 3:54-59. 10.1016/S1367-5931(99)80010-6, 10021399.
21. Camarero S, Pardo I, Cañas AI, Molina P, Record E, Martínez AT, Martínez MJ, Alcalde M. Engineering platforms for directed evolution of laccase from Pycnoporus cinnabarinus. Appl Environ Microbiol 2012, 78:1370-1384. 10.1128/AEM.07530-11, 3294479, 22210206.
22. Maté D, García-Burgos C, García-Ruiz E, Ballesteros A, Camarero S, Alcalde M. Laboratory evolution of high redox potential laccases. Chem Biol 2010, 17:1030-1041. 10.1016/j.chembiol.2010.07.010, 20851352.
23. Pardo I, Vicente AI, Mate DM, Alcalde M, Camarero S. Development of chimeric laccases by directed evolution. Biotechnol Bioeng 2012, 109:2978-2986. 10.1002/bit.24588, 22729887.
24. Ruiz-Dueñas FJ, Morales M, García E, Miki Y, Martínez MJ, Martínez AT. Substrate oxidation sites in versatile peroxidase and other basidiomycete peroxidases. J Exp Bot 2009, 60:441-452. 10.1093/jxb/ern261, 18987391.
25. Bidlack J, Malone M, Benson R. Molecular structure and component integration of secondary cell walls in plants. Proc Okla Acad Sci 1992, 72:51-56.
26. Camarero S, Cañas AI, Nousiainen P, Record E, Lomascolo A, Martínez MJ, Martínez AT. p-Hydroxycinnamic acids as natural mediators for laccase oxidation of recalcitrant compounds. Environ Sci Technol 2008, 42:6703-6709. 10.1021/es8008979, 18800552.
27. Gutiérrez A, Rencoret J, Ibarra D, Molina S, Camarero S, Romero J, del Río JC, Martínez AT. Removal of lipophilic extractives from paper pulp by laccase and lignin-derived phenols as natural mediators. Environ Sci Technol 2007, 41:4124-4129. 10.1021/es062723+, 17612200.
28. Lacki K, Duvnjak Z. Transformation of 3,5-dimethoxy,4-hydroxy cinnamic acid by polyphenol oxidase from the fungus Trametes versicolor: product elucidation studies. Biotechnol Bioeng 1998, 57:694-703. 10.1002/(SICI)1097-0290(19980320)57:6<694::AID-BIT7>3.0.CO;2-G, 10099249.
29. Shin K-S. Oxidation of syringic acid by extracellular peroxidase of white-rot fungus, Pleurotus ostreatus. Mycoscience 1995, 36:31-35.
30. Rosado T, Bernardo P, Koci K, Coelho AV, Robalo MP, Martins LO. Methyl syringate: an efficient phenolic mediator for bacterial and fungal laccases. Bioresour Technol 2012, 124:371-378.
31. Zumárraga M, Bulter T, Shleev S, Polaina J, Martinez-Arias A, Plou FJ, Ballesteros A, Alcalde M. In vitro evolution of a fungal laccase in high concentrations of organic cosolvents. Chem Biol 2007, 14:1052-1064. 10.1016/j.chembiol.2007.08.010, 17884637.
32. Li KC, Xu F, Eriksson KEL. Comparison of fungal laccases and redox mediators in oxidation of a nonphenolic lignin model compound. Appl Environ Microbiol 1999, 65:2654-2660. 91392, 10347057.
33. Fillat U, Prieto A, Camarero S, Martínez AT, Martínez MJ. Biodeinking of flexographic inks by fungal laccases using synthetic and natural mediators. Biochem Eng J 2012, 67:97-103.
34. Babot ED, Rico A, Rencoret J, Kalum L, Lund H, Romero J, del Río JC, Martínez AT, Gutiérrez A. Towards industrially feasible delignification and pitch removal by treating paper pulp with Myceliophthora thermophila laccase and a phenolic mediator. Bioresour Technol 2011, 102:6717-6722. 10.1016/j.biortech.2011.03.100, 21511459.
35. Sharma P, Goel R, Capalash N. Bacterial laccases. World J Microbiol Biotechnol 2007, 23:823-832.
36. Cambria MT, Gullotto D, Garavaglia S, Cambria A. In silico study of structural determinants modulating the redox potential of Rigidoporus lignosus and other fungal laccases. J Biomol Struct Dyn 2012, 30:89-101. 10.1080/07391102.2012.674275, 22571435.
37. Kim H, Mickel M, Hampp N. Molecular origin of the stability of violuric acid radicals at high pH-values. Chem Phys Lett 2003, 371:410-416.
38. Leermakers PA, Hoffman WA. Chelates of violuric acid. J Am Chem Soc 1958, 80:5663-5667.
39. Drumond FM, Junqueira D, Palma De Oliveira D. Azo Dyes and Their Metabolites: Does the Discharge of the Azo Dyeinto Water Bodies Represent Humanand Ecological Risks?. Advances in Treating Textile Effluent Hause P, doi:10.5772/19872http://www.intechopen.com/books/advances-in-treating-textile-effluent/azo-dyes-and-their-metabolites-does-the-discharge-of-the-azo-dye-into-water-bodies-represent-human-aISBN 978-953-307-704-8.
40. Zille A, Ramalho P, Tzanov T, Millward R, Aires V, Cardoso MH, Ramalho MT, Gübitz GM, Cavaco-Paulo A. Predicting dye biodegradation from redox potentials. Biotechnol Prog 2004, 20:1588-1592. 10.1021/bp049963i, 15458349.
41. Chivukula M, Renganathan V. Phenolic azo dye oxidation by laccase from Pyricularia oryzae. Appl Environ Microbiol 1995, 61:4374-4377. 1388656, 16535191.
42. Champagne PP, Ramsay JA. Dye decolorization and detoxification by laccase immobilized on porous glass beads. Bioresour Technol 2010, 101:2230-2235. 10.1016/j.biortech.2009.11.066, 20015643.
43. Brissos V, Pereira L, Munteanu F-D, Cavaco-Paulo A, Martins LO. 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. 10.1002/biot.200800248, 19156728.
44. Lin WZ, Navaratnam S, Yao SD, Lin NY. Antioxidative properties of hydroxycinnamic acid derivatives and a phenylpropanoid glycoside. A pulse radiolysis study. Radiat Phys Chem 1998, 53:425-430.
45. Moodley B, Mulholland DA, Brookes HC. The electro-oxidation of lignin in Sappi Saiccor dissolving pulp mill effluent. Water Sa 2011, 37:33-40.
46. Aaby K, Hvattum E, Skrede G. Analysis of flavonoids and other phenolic compounds using high-performance liquid chromatography with coulometric array detection: relationship to antioxidant activity. J Agric Food Chem 2004, 52:4595-4603. 10.1021/jf0352879, 15264888.
47. Xu F, Berka RM, Wahleithner JA, Nelson BA, Shuster JR, Brown SH, Palmer AE, Solomon EI. Site-directed mutations in fungal laccase: effect on redox potential, activity and pH profile. Biochem J 1998, 334:63-70. 1219662, 9693103.