Novel laccase-like multicopper oxidases from the Myrothecium roridum fungus - production enhancement, identification and application in the dye removal process

• Authors: Anna Jasińska , Aleksandra Góralczyk , Adrian Soboń , Jerzy Długoński
• Languages of publication: EN

Abstracts

EN

The aim of this study was to overproduce, identify and apply novel laccase-like multicopper oxidases (LMCOs) from Myrothecium roridum in a dye removal process. LMCOs' production was enhanced by modifying the medium and adding copper ions. After purification, two proteins, LMCO1 and LMCO2, with molecular masses of 46.7 and 66.3 kDa were discovered. Peptide analysis by mass spectrometry revealed that they belong to the cupredoxin superfamily. Characteristic peptide sequences were obtained for MCOs and bilirubin oxidases. Crude enzymes were applied in a dye decolorization process. Supplementation with 1 mM of vanillin allowed an almost complete elimination of the Indigo carmine within 3 hours. The dye was removed from a solution containing metals, surfactants and organic solvents. The in-gel assessment of the activity and decolorization ability of MCOs, followed by protein extraction and SDS-PAGE, confirmed that only LMCO2 was responsible for the dye removal. MCOs produced by Myrothecium sp. have been poorly studied before. The obtained results broaden knowledge on this subject and may contribute to the development of an eco-friendly method of dye elimination.

Keywords

EN

multicopper oxidases; laccase; bilirubin oxidase; Myrothecium roridum; decolorization

• Publisher: Polish Biochemical Society
• Journal: Acta Biochimica Polonica
• Year: 2018
• Volume: 65
• Issue: 2
• Pages: 287-295

Dates

published

2018

received

2017-12-19

revised

2018-03-13

accepted

2018-03-19

(unknown)

2018-04-25

Contributors

author

Anna Jasińska

• Department of Industrial Microbiology and Biotechnology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, Poland

author

Aleksandra Góralczyk

• Department of Industrial Microbiology and Biotechnology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, Poland

author

Adrian Soboń

• Department of Industrial Microbiology and Biotechnology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, Poland

author

Jerzy Długoński

• Department of Industrial Microbiology and Biotechnology, Faculty of Biology and Environmental Protection, University of Lodz, Łódź, Poland

References

• Ahmed MA, Brick AA, Mohamed AA (2017) An efficient adsorption of indigo carmine dye from aqueous solution on mesoporous Mg/Fe layered double hydroxide nanoparticles prepared by controlled sol-gel route. Chemosphere 174: 280-288.
• Baldrian P, Gabriel J (2002) Copper and cadmium increase laccase activity in Pleurotus ostreatus. FEMS Microbiol Lett 206: 69-74.doi: 10.1016/S0378-1097(01)00519-5.
• Beloqui A, Pita M, Polaina J, Martínez-Arias A, Golyshina OV, Zumárraga M, Yakimov MM, García-Arellano H, Alcalde M, Fernández VM, Elborough K, Andreu JM, Ballesteros A, Plou FJ, Timmis KN, Ferrer M, Golyshin PN (2006) Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships. J Biol Chem 281: 22933-22942.doi: 10.1074/jbc.M600577200.
• Camarero S, Ibarra D, Martínez MJ, Martínez AT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Environ Microbiol 71: 1775-1784.doi: 10.1128/AEM.71.4.1775-1784.2005.
• Campos PA, Levin LN, Wirth SA (2016) Heterologous production, characterization and dye decolorization ability of a novel thermostable laccase isoenzyme from Trametes trogii BAFC 463. Process Biochem 51: 895-903.doi: 10.1016/j.procbio.2016.03.015
• Chen S, Ma D, Ge W, Buswell JA (2003) Induction of laccase activity in the edible straw mushroom, Volvariella volvacea. FEMS Microbiol Lett 218: 143-148.doi: 10.1016/S0378-1097(02)01131-X.
• Desai S, Nityanand C (2011) Microbial laccases and their applications: a review. Asian J Biotech 3: 98-124.doi: 10.3923/ajbkr.2011.98.124
• Dogdu G, Yalcuk A (2016) Indigo dyeing wastewater treatment by eco-friendly constructed wetlands using different bedding media. Desal Water Treat 57: 15007-15019.doi: 10.1080/19443994.2015.1070290
• D'Souza DT, Tiwari R, Sah AK, Raghukumar C (2006) Enhanced production of laccase by a marine fungus during treatment of colored effluents and synthetic dyes. Enzyme Microb Tech 38: 504-511.doi: 10.1016/j.enzmictec.2005.07.005
• Durand F, Kjaergaard CH, Suraniti E, Gounel S, Hadt RG, Solomon EI, Mano N (2012) Bilirubin oxidase from Bacillus pumilus: a promising enzyme for the elaboration of efficient cathodes in biofuel cells. Biosens Bioelectron 35: 140-146.doi: 10.1016/j.bios.2012.02.033.
• Eggert C, Temp U, Dean JF, Eriksson KE (1996) A fungal metabolite mediates degradation of non-phenolic lignin structures and synthetic lignin by laccase. FEBS Lett 391: 144-148.doi: 10.1016/0014-5793(96)00719-3.
• Galhaup C, Goller S, Peterbauer CK, Strauss J, Haltrich D (2002) Characterization of the major laccase isoenzyme from Trametes pubescens and regulation of its synthesis by metal ions. Microbiology 148: 2159-2169.doi: 10.1099/00221287-148-7-2159.
• Galhaup C, Haltrich D (2001) Enhanced formation of laccase activity by the white-rot fungus Trametes pubescens in the presence of copper. Appl Microbiol Biotechnol 56: 225-232.doi: 10.1007/s002530100636.
• Gomaa OM, Momtaz OA (2015) Copper induction and differential expression of laccase in Aspergillus flavus. Braz J Microbiol 46: 285-292.doi: 10.1590/S1517-838246120120118.
• Gupta VK, Khamparia S, Tyagi I, Jaspal D, Malviya A (2015) Decolorization of Mixture of Dyes: A Critical Review. Global J Environ Sci Manage 1: 71-94.doi: 10.7508/gjesm.2015.01.007
• 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.doi: 10.1111/j.1742-4658.2006.05247.x.
• Hou H, Zhou J, Wang J, Du C, Yan B (2004) Enhancement of laccase production by Pleurotus ostreatus and its use for the decolorization of anthraquinone dye. Process Biochem 39: 1415-1419.doi: 10.1016/S0032-9592(03)00267-X
• Iracheta-Cárdena MM, Rocha-Peña MA, Galán-Wong LJ, Arévalo-Niño K, Tovar-Herrera OE (2016) A Pycnoporus sanguineus laccase for denim bleaching and its comparison with an enzymatic commercial formulation. J Environ Manage 177: 93-100.doi: 10.1016/j.jenvman.2016.04.008.
• Jasińska A, Bernat P, Paraszkiewicz K (2013) Malachite Green removal from aqueous solution using the system rapeseed press cake and fungus Myrothecium roridum. Desalin Water Treat 51: 7663-7671.doi: 10.1080/19443994.2013.779939
• Jasińska A, Góralczyk A, Długoński J (2016) Dye decolorization and degradation by microorganisms. In: Microbial Biodegradation: From Omics to Function and Application. Długoński J ed, pp.119-141, Caister Academic Press, Norfolk.doi: 10.21775/9781910190456.08
• Jasińska A, Paraszkiewicz K, Sip A, Długoński J (2015) Malachite Green decolorization by the filamentous fungus Myrothecium roridum- Mechanistic study and process optimization. Bioresour Technol 194: 43-48.doi: 10.1016/j.biortech.2015.07.008.
• Jasińska A, Różalska S, Bernat P, Paraszkiewicz K, Długoński J (2012) Malachite Green decolorization by non-basidiomycete filamentous fungi of Penicillium pinophilum and Myrothecium roridum. Int Biodeter Biodegr 73: 33-40.doi: 10.1016/j.ibiod.2012.06.025
• Jin X, Yu X, Zhu G, Zheng Z, Feng F, Zhang Z (2016) Conditions Optimizing and Application of Laccase-mediator System (LMS) for the Laccase-catalyzed Pesticide Degradation. Sci Rep 6: 35787.doi: 10.1038/srep35787.
• Karp SG, Faraco V, Amore A, Letti LA, Soccol VT, Soccol CR (2015) Statistical optimization of laccase production and delignification of sugarcane bagasse by Pleurotus ostreatus in solid-state fermentation. BioMed Res Int doi: 10.1155/2015/181204.
• Levin L, Herrmann C, Papinutti VL (2008) Optimization of lignocellulolytic enzyme production by the white-rot fungus Trametes trogii in solid-state fermentation using response surface methodology. Biochem Eng J 39: 207-214.doi: 10.1016/j.bej.2007.09.004
• Li HX, Zhang RJ, Tang L, Zhang JH, Mao ZG (2014) In vivo and in vitro decolorization of synthetic dyes by laccase from solid state fermentation with Trametes sp. SYBC-L4. Bioprocess Biosyst Eng 37: 2597-2605.doi: 10.1007/s00449-014-1237-y.
• Lu R, Ma L, He F, Yu D, Fan R, Zhang Y, Long Z, Zhang X, Yang Y (2016) White-rot fungus Ganoderma sp.En3 had a strong ability to decolorize and tolerate the anthraquinone, indigo and triphenylmethane dye with high concentrations. Bioprocess Biosyst Eng 39: 381-390.doi: 10.1007/s00449-015-1521-5.
• Majeau JA, Brar SK, Tyagi RD (2010) Laccases for removal of recalcitrant and emerging pollutants. Bioresour Technol 101: 2331-2350.doi: 10.1016/j.biortech.2009.10.087.
• Manel MK, Hela ZM, Lassaad B, Steve W, Tahar M (2009) Malachite Green decolourization and detoxification by the laccase from a newly isolated strain of Trametes sp. Int Biodeterior Biodeg 63: 600-606.doi: 10.1016/j.ibiod.2009.04.003
• Martins LO, Soares CM, Pereira MM, Teixeira M, Costa T, Jones GH, Henriques AO (2002) Molecular and biochemical characterization of a highly stable bacterial laccase that occurs as a structural component of the Bacillus subtilis endospore coat. J Biol Chem 277: 18849-18859.doi: 10.1074/jbc.M200827200.
• Murugesan K, Nam I-H, Kim Y-M, Chang Y-S (2007) Decolorization of reactive dyes by a thermostable laccase produced by Ganoderma lucidum in solid state culture. Enz Microb Technol 40: 1662-1672.doi: 10.1016/j.enzmictec.2006.08.028
• Palmieri G, Bianco C, Cennamo G, Giardina P, Marino G, Monti M, Sannia G (2001) Purification, characterization, and functional role of a novel extracellular protease from Pleurotus ostreatus. Appl Environ Microbiol 67: 2754-2759.doi: 10.1128/AEM.67.6.2754-2759.2001.
• Paz A, Carballo J, Pérez MJ, Domínguez JM (2017) Biological treatment of model dyes and textile wastewaters. Chemosphere 181: 168-177.doi: 10.1016/j.chemosphere.2017.04.046.
• Piscitelli A, Giardina P, Lettera V, Pezzella C, Sannia G, Faraco V (2011) Induction and transcriptional regulation of laccases in fungi. Curr Genomics 12: 104-112.doi: 10.2174/138920211795564331.
• Reiss R, Ihssen J, Richter M, Eichhorn E, Schilling B, Thöny-Meyer L (2013) Laccase versus laccase-like multi-copper oxidase: A comparative study of similar enzymes with diverse substrate spectra. PLOS ONE 8: e65633.doi: 10.1371/journal.pone.0065633.
• Sakasegawa SI, Ishikawa H, Imamura S, Sakuraba H, Goda S, Ohshima T (2006) Bilirubin oxidase activity of Bacillus subtilis CotA. Appl Environ Microbiol 72: 972-975.doi: 10.1128/AEM.72.1.972-975.2006.
• Sakurai T, Kataoka K (2007) Basic and applied features of multicopper oxidases, CueO, bilirubin oxidase, and laccase. Chem Rec 7: 220-229.doi: 10.1002/tcr.20125.
• Sarayu K, Sandhya S (2012) Current Technologies for Biological Treatment of Textile Wastewater-A Review. Appl Biochem Biotechnol 167: 645–661.doi: 10.1007/s12010-012-9716-6.
• Sivakumar R, Rajendran R, Balakumar C, Tamilvendan M (2010) Isolation, screening and optimization of production medium for thermostable laccase production from Ganoderma sp. Int J Environ Sci Tech 2: 7133-7141.doi: 10.20546/ijcmas.2017.604.289
• Soboń A, Szewczyk R, Długoński J (2016) Tributyltin (TBT) biodegradation induces oxidative stress of Cunninghamella echinulate. Int Biodeterior Biodegr 107: 92-101.doi: 10.1016/j.ibiod.2015.11.013
• Sulistyaningdyah WT, Ogawa J, Tanaka H, Maeda C, Shimizu S (2004) Characterization of alkaliphilic laccase activity in the culture supernatant of Myrothecium verrucaria 24G-4 in comparison with bilirubin oxidase. FEMS Microbiol Lett 230: 209-214.doi: 10.1016/S0378-1097(03)00892-9.
• Szewczyk R, Soboń A, Słaba M, Długoński J (2015) Mechanism study of alachlor biodegradation by Paecilomyces marquandii with proteomic and metabolomic methods. J Hazard Mater 291: 52-64.doi: 10.1016/j.jhazmat.2015.02.063.
• Vasina DV, Mustafaev ON, Moiseenko KV, Sadovskaya NS, Glazunova OA, Tyurin AA, Fedorova TV, Pavlov AR, Tyazhelova TV, Goldenkova-Pavlova IV, Koroleva OV (2015) The Trametes hirsuta 072 laccase multigene family: Genes identification and transcriptional analysis under copper ions induction. Biochimie 116: 154-164.doi: 10.1016/j.biochi.2015.07.015.
• Xu Y, Lu Y, Zhang R, Wang H, Liu Q (2016) Characterization of a novel laccase purified from the fungus Hohenbuehelia serotina and its decolourisation of dyes. Acta Biochim Pol 63: 273-279.doi: 10.18388/abp.2015_1091.
• Zhao D, Zhang X, Cui D, Zhao M (2012) Characterisation of a novel white laccase from the Deuteromycete fungus Myrothecium verrucaria NF-05 and its decolourisation of dyes. PLoS One doi: 10.1371/journal.pone.0038817.
• Zilly A, Coelho-Moreira JD, Bracht A, de Souza CGM, Carvajal AE, Koehnlein EA, Peralta RM (2011) Influence of NaCl and Na2SO4 on the kinetics and dye decolorization ability of crude laccase from Ganoderma lucidum. Int Biodeterior Biodegr 65: 340-344.doi: 10.1016/j.ibiod.2010.12.007

Identifiers

DOI

10.18388/abp.2017_2546