Laccase of Agaricus subrufescens cultivated with sugarcane molasses promotes the decolorization of synthetic dyes

Authors

DOI:

https://doi.org/10.33448/rsd-v9i12.10942

Keywords:

Agaricus blazei; Agro-industrial waste; Basidiomycota; Biodegradation; Textile dyes.

Abstract

Agaricus subrufescens is a mushroom that produces laccase oxidoreductases that degrade dyes. Cultivation conditions such as nitrogen concentration, carbon source, and inducers can increase laccase production. This study aimed to cultivate A. subrufescens with urea, agro-industrial by-products, and inducers to produce laccase for dyes decolorization. Agaricus subrufescens U7-1 and U7-3 were grown in liquid medium with urea (0, 2, 4, 6, and 8 g L-1), carbon sources (glucose, sugarcane molasses - SuM and soybean molasses - SoM), and inducers (ethanol, guaiacol, vanillin, and veratryl alcohol). The enzymatic extract of the culture was used in the decolorization of remazol brilliant blue R (RBBR), reactive black 5 (RB5), and malachite green (MG). The laccase production of A. subrufescens was inversely proportional to the urea concentration and the greater U7-1 laccase activity occurred with 2 g L-1 urea and U7-3 produced more laccase without urea. SuM increased the laccase activity and anticipated the laccase peak of U7-1 in five days and U7-3 in 15 days. SoM reduced laccase activity. Vanillin increased the laccase activity of U7-1 by 29% (44380 U L-1) and anticipated activity peak; and vanillin and veratryl alcohol increased the laccase activity (44770 U L-1) of U7-3, but delayed activity peak. The extracts of U7-1 and U7-3 obtained from the vanillin culture discolored the RBBR in 24 h (65% and 75%), and VM (70%, 24 and 72 h), but did not reduce the color of PR5.

References

Al Loman, A., & Ju, L. K. (2016). Soybean carbohydrate as fermentation feedstock for production of biofuels and value-added chemicals. Process Biochemistry, 51(8), 1046-1057.

Almeida, P. H., Oliveira, A. C. C., Souza, G. P. D., Friedrich, J. C., Linde, G. A., Colauto, N. B., & Valle, J. S. (2018). Decolorization of remazol brilliant blue R with laccase from Lentinus crinitus grown in agro-industrial by-products. Anais da Academia Brasileira de Ciências, 90(4), 3463-3473.

Aragão, M. S., Menezes, D. B., Ramos, L. C., Oliveira, H. S., Bharagava, R. N., Ferreira, L. F. R., Teixeira, J.A., Ruzene, D.S., & Silva, D. P. (2020). Mycoremediation of vinasse by surface response methodology and preliminary studies in air-lift bioreactors. Chemosphere, 244, 125432.

Arakaki, A. H., Souza Vandenberghe, L. P. D., Soccol, V. T., Masaki, R., Rosa Filho, E. F. D., Gregório, A., & Soccol, C. R. (2011). Optimization of biomass production with copper bioaccumulation by yeasts in submerged fermentation. Brazilian Archives of Biology and Technology, 54(5), 1027-1034.

Bertéli, M. B. D., Umeo, S. H., Bertéli, A., Valle, J. S., Linde, G. A., & Colauto, N. B. (2014). Mycelial antineoplastic activity of Agaricus blazei. World Journal of Microbiology and Biotechnology, 30(8), 2307-2313.

Bertéli, M. B., Lopes, A. D., Colla, I. M., Linde, G. A., & Colauto, N. B. (2016). Agaricus subrufescens: substratum nitrogen concentration and mycelial extraction method on antitumor activity. Anais da Academia Brasileira de Ciências, 88(4), 2239-2246.

Chatha, S. A. S., Asgher, M., & Iqbal, H. M. (2017). Enzyme-based solutions for textile processing and dye contaminant biodegradation—a review. Environmental Science and Pollution Research, 24(16), 14005-14018.

Cheng, C., Zhou, Y., Lin, M., Wei, P., & Yang, S. T. (2017). Polymalic acid fermentation by Aureobasidium pullulans for malic acid production from soybean hull and soy molasses: fermentation kinetics and economic analysis. Bioresource Technology, 223, 166-174.

Colauto, N.B., Silveira, A.R., Eira, A.F., & Linde, G.A. (2010). Alternative to peat for Agaricus brasiliensis yield. Bioresource Technology, 101(2), 712-716.

Collins, P. J., & Dobson, A. (1997). Regulation of laccase gene transcription in Trametes versicolor. Applied and Environmental Microbiology, 63(9), 3444-3450.

CONAB, 2020. - COMPANHIA NACIONAL DE ABASTECIMENTO. Levantamento da safra de cana-de-açúcar (área plantada, produtividade e produção). Disponível em http://www.conab.gov.br (Acesso em 05 dez. 2020).

Costa, M. C. D., Regina, M., Cilião Filho, M., Linde, G. A., Do Valle, J. S., Paccola-Meirelles, L. D., & Colauto, N. B. (2015). Photoprotective and antimutagenic activity of Agaricus subrufescens basidiocarp extracts. Current Microbiology, 71(4), 476-482.

D'Agostini, É. C., Mantovani, T. R. D. A., Valle, J. S. D., Paccola-Meirelles, L. D., Colauto, N. B., & Linde, G. A. (2011). Low carbon/nitrogen ratio increases laccase production from basidiomycetes in solid substrate cultivation. Scientia Agricola, 68(3), 295-300.

Eggert, C., Temp, U., Dean, J. F., & Eriksson, K. E. L. (1995). Laccase‐mediated formation of the phenoxazinone derivative, cinnabarinic acid. FEBS letters, 376(3), 202-206.

Eichlerová, I., Homolka, L., Benada, O., Kofroňová, O., Hubálek, T., & Nerud, F. (2007). Decolorization of orange G and Remazol Brilliant Blue R by the white rot fungus Dichomitus squalens: Toxicological evaluation and morphological study. Chemosphere, 69(5), 795-802.

Elisashvili, V., & Kachlishvili, E. (2009). Physiological regulation of laccase and manganese peroxidase production by white-rot Basidiomycetes. Journal of Biotechnology, 144(1), 37-42.

Elisashvili, V., Kachlishvili, E., & Asatiani, M. D. (2018). Efficient production of lignin-modifying enzymes and phenolics removal in submerged fermentation of olive mill by-products by white-rot basidiomycetes. International Biodeterioration & Biodegradation, 134, 39-47.

Elisashvili, V., Kachlishvili, E., & Penninckx, M. (2008). Effect of growth substrate, method of fermentation, and nitrogen source on lignocellulose-degrading enzymes production by white-rot basidiomycetes. Journal of Industrial Microbiology & Biotechnology, 35(11), 1531-1538.

Elisashvili, V., Kachlishvili, E., Asatiani, M. D., Darlington, R., & Kucharzyk, K. H. (2017). Physiological peculiarities of lignin-modifying enzyme production by the white-rot basidiomycete Coriolopsis gallica strain BCC 142. Microorganisms, 5(4), 73.

Fabrini, F. F., Avelino, K. V., Marim, R. A., Cardoso, B. K., Colauto, G. A. L., Colauto, N. B., & do Valle, J. S. (2016). Produção de lacase de Pycnoporus sanguineus em meio de cultivo à base de melaço soja. Arquivos de Ciências Veterinárias e Zoologia da UNIPAR, 19(3), 159-164.

Feltrin, V. P., Sant'Anna, E. S., Porto, A. C. S., & Torres, R. C. O. (2000). Lactobacillus plantarum production with sugarcane molasses. Brazilian Archives of Biology and Technology, 43(1), 119-124.

Fernández-López, C. L., Torrestiana-Sánchez, B., Salgado-Cervantes, M. A., García, P. M., & Aguilar-Uscanga, M. G. (2012). Use of sugarcane molasses “B” as an alternative for ethanol production with wild-type yeast Saccharomyces cerevisiae ITV-01 at high sugar concentrations. Bioprocess and Biosystems Engineering, 35(4), 605-614.

Giardina, P., Faraco, V., Pezzella, C., Piscitelli, A., Vanhulle, S., & Sannia, G. (2010). Laccases: a never-ending story. Cellular and Molecular Life Sciences, 67(3), 369-385.

Glazunova, O. A., Trushkin, N. A., Moiseenko, K. V., Filimonov, I. S., & Fedorova, T. V. (2018). Catalytic efficiency of basidiomycete laccases: redox potential versus substrate-binding pocket structure. Catalysts, 8(4), 152.

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 Biochemistry, 39(11), 1415-1419.

Hsu, C. A., Wen, T. N., Su, Y. C., Jiang, Z. B., Chen, C. W., & Shyur, L. F. (2012). Biological degradation of anthroquinone and azo dyes by a novel laccase from Lentinus sp. Environmental Science & Technology, 46(9), 5109-5117.

Largeteau, M. L., Llarena-Hernández, R. C., Regnault-Roger, C., & Savoie, J. M. (2011). The medicinal Agaricus mushroom cultivated in Brazil: biology, cultivation and non-medicinal valorisation. Applied Microbiology and Biotechnology, 92(5), 897-907.

Marim, R. A., Oliveira, A. C. C., Marquezoni, R. S., Servantes, J. P. R., Cardoso, B. K., Linde, G. A., Colauto, N.B., & Valle, J. S. (2016). Use of sugarcane molasses by Pycnoporus sanguineus for the production of laccase for dye decolorization. Genetics and Molecular Research, 15, gmr15048972.

Martani, F., Beltrametti, F., Porro, D., Branduardi, P., & Lotti, M. (2017). The importance of fermentative conditions for the biotechnological production of lignin modifying enzymes from white-rot fungi. FEMS Microbiology Letters, 364(13), fnx134.

Martínková, L., Kotik, M., Marková, E., & Homolka, L. (2016). Biodegradation of phenolic compounds by Basidiomycota and its phenol oxidases: a review. Chemosphere, 149, 373-382.

Meniqueti, A. B., Ruiz, S. P., Faria, M. G. I., do Valle, J. S., Gonçalves Jr, A. C., Dragunski, D. C., Colauto, N.B., & Linde, G. A. (2020). Iron-enriched mycelia of edible and medicinal basidiomycetes. Environmental Technology, 29, 1-7.

Mikiashvili, N., Wasser, S. P., Nevo, E., & Elisashvili, V. (2006). Effects of carbon and nitrogen sources on Pleurotus ostreatus ligninolytic enzyme activity. World Journal of Microbiology and Biotechnology, 22(9), 999-1002.

Morales-Álvarez, E. D., Rivera-Hoyos, C. M., Poveda-Cuevas, S. A., Reyes-Guzmán, E. A., Pedroza-Rodríguez, A. M., Reyes-Montaño, E. A., & Poutou-Piñales, R. A. (2018). Malachite green and crystal violet decolorization by Ganoderma lucidum and Pleurotus ostreatus supernatant and by rGlLCC1 and rPOXA 1B concentrates: molecular docking analysis. Applied Biochemistry and Biotechnology, 184(3), 794-805.

Morozova, O. V., Shumakovich, G. P., Shleev, S. V., & Yaropolov, Y. I. (2007). Laccase-mediator systems and their applications: a review. Applied Biochemistry and Microbiology, 43(5), 523-535.

Morsy, S. A. G. Z., Ahmad Tajudin, A., Ali, M., Mohamad, S., & Shariff, F. M. (2020). Current development in decolorization of synthetic dyes by immobilized laccases. Frontiers in Microbiology, 11, 2350.

Myasoedova, N. M., Chernykh, A. M., Psurtseva, N. V., Belova, N. V., & Golovleva, L. A. (2008). New efficient producers of fungal laccases. Applied Biochemistry and Microbiology, 44(1), 73-77.

Nakade, K., Nakagawa, Y., Yano, A., Sato, T., & Sakamoto, Y. (2010). Characterization of an extracellular laccase, PbLac1, purified from Polyporus brumalis. Fungal Biology, 114(8), 609-618.

Oliveira, J. M., Michelon, M., & Burkert, C. A. V. (2020). Biotechnological potential of soybean molasses for the production of extracellular polymers by diazotrophic bacteria. Biocatalysis and Agricultural Biotechnology, 101609.

Palmieri, G., Giardina, P., Bianco, C., Fontanella, B., & Sannia, G. (2000). Copper induction of laccase isoenzymes in the ligninolytic fungus Pleurotus ostreatus. Applied and Environmental Microbiology, 66(3), 920-924.

Pereira, A. S., Shitsuka, D. M., Parreira, F. B., & Shitsuka, R. (2018). Metodologia da pesquisa científica [recurso eletrônico[eBook]. Santa Maria. Ed. UAB/NTE/UFSM. Recuperado de https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computa cao_MetodologiaPesquisa-Cientifica.pdf?sequence=1.

Piscitelli, A., Giardina, P., Lettera, V., Pezzella, C., Sannia, G., & Faraco, V. (2011). Induction and transcriptional regulation of laccases in fungi. Current Genomics, 12(2), 104-112.

Pype, R., Flahaut, S., & Debaste, F. (2019). On the importance of mechanisms analysis in the degradation of micropollutants by laccases: The case of Remazol Brilliant Blue R. Environmental Technology & Innovation, 14, 100324.

Rodrigues, E. M., Karp, S. G., Malucelli, L. C., Helm, C. V., & Alvarez, T. M. (2019). Evaluation of laccase production by Ganoderma lucidum in submerged and solid‐state fermentation using different inducers. Journal of Basic Microbiology, 59(8), 784-791.

Rodriguez-Couto, S. (2013). Treatment of textile wastewater by white-rot fungi: still a far away reality. Textiles and Light Industrial Science and Technology, 2(3), 113-119.

Romão, B. B., da Silva, F. B., de Resende, M. M., & Cardoso, V. L. (2012). Ethanol production from hydrolyzed soybean molasses. Energy & Fuels, 26(4), 2310-2316.

Rubel, R., Dalla Santa, H. S., Dos Santos, L. F., Fernandes, L. C., Figueiredo, B. C., & Soccol, C. R. (2018). Immunomodulatory and antitumoral properties of Ganoderma lucidum and Agaricus brasiliensis (Agaricomycetes) medicinal mushrooms. International Journal of Medicinal Mushrooms, 20(4), 393-403.

Santana, T. T., Linde, G. A., Colauto, N. B., & do Valle, J. S. (2018). Metallic-aromatic compounds synergistically induce Lentinus crinitus laccase production. Biocatalysis and Agricultural Biotechnology, 16, 625-630.

Santos, A. Z., Cândido Neto, J. M., Granhen Tavares, C. R., & Gomes da Costa, S. M. (2004). Screening of filamentous fungi for the decolorization of a commercial reactive dye. Journal of Basic Microbiology, 44(4), 288-295.

Scheid, S. S., Faria, M. G. I., Velasquez, L. G., do Valle, J. S., Gonçalves, A. C., Dragunski, D. C., Colauto, N.B., & Linde, G. A. (2020). Iron biofortification and availability in the mycelial biomass of edible and medicinal basidiomycetes cultivated in sugarcane molasses. Scientific reports, 10(1), 1-6.

Sen, S. K., Raut, S., Bandyopadhyay, P., & Raut, S. (2016). Fungal decolouration and degradation of azo dyes: a review. Fungal Biology Reviews, 30(3), 112-133.

Siqueira, P. F., Karp, S. G., Carvalho, J. C., Sturm, W., Rodríguez-León, J. A., Tholozan, J. L., Singhania, R.R., Pandey, A., & Soccol, C. R. (2008). Production of bio-ethanol from soybean molasses by Saccharomyces cerevisiae at laboratory, pilot and industrial scales. Bioresource Technology, 99(17), 8156-8163.

Songulashvili, G., Spindler, D., Jimenez-Tobon, G. A., Jaspers, C., Kerns, G., & Penninckx, M. J. (2015). Production of a high level of laccase by submerged fermentation at 120-L scale of Cerrena unicolor C-139 grown on wheat bran. Comptes Rendus Biologies, 338(2), 121-125.

Ullrich, R., Dung, N. L., & Hofrichter, M. (2005). Laccase from the medicinal mushroom Agaricus blazei: production, purification and characterization. Applied Microbiology and Biotechnology, 67(3), 357-363.

Umeo, S. H., Faria, M. G. I., Vilande, S. S. S., Dragunski, D. C., do Valle, J. S., Colauto, N. B., & Linde, G. A. (2019). Iron and zinc mycelial bioaccumulation in Agaricus subrufescens strains. Semina: Ciências Agrárias, 40(6), 2513-2522.

Umeo, S. H., Souza, G. P. N., Rapachi, P. M., Garcia, D. M., Paccola-Meirelles, L. D., Valle, J. S., Colauto, N.B., & Linde, G. A. (2015). Screening of basidiomycetes in submerged cultivation based on antioxidant activity. Genetics and Molecular Research, 14(3), 9907-9914.

Upadhyay, P., Shrivastava, R., & Agrawal, P. K. (2016). Bioprospecting and biotechnological applications of fungal laccase. 3 Biotech, 6(1), 15.

Valle, J. S., Vandenberghe, L. P. S., Santana, T. T., Linde, G. A., Colauto, N. B., & Soccol, C. R. (2014). Optimization of Agaricus blazei laccase production by submerged cultivation with sugarcane molasses. African Journal of Microbiology Research, 8(9), 939-946.

Valle, J. S., Vandenberghe, L. P. S., Oliveira, A. C. C., Tavares, M. F., Linde, G. A., Colauto, N. B., & Soccol, C. R. (2015). Effect of different compounds on the induction of laccase production by Agaricus blazei. Genetics and Molecular Research, 14(4), 15882-15891.

Vijayalaxmi, S., Jayalakshmi, S. K., & Sreeramulu, K. (2015). Polyphenols from different agricultural residues: extraction, identification and their antioxidant properties. Journal of Food Science and Technology, 52(5), 2761-2769.

Vikrant, K., Giri, B. S., Raza, N., Roy, K., Kim, K. H., Rai, B. N., & Singh, R. S. (2018). Recent advancements in bioremediation of dye: current status and challenges. Bioresource Technology, 253, 355-367.

Wisitrassameewong, K., Karunarathna, S. C., Thongklang, N., Zhao, R., Callac, P., Moukha, S., Férandon, C., Chukeatirote, E., & Hyde, K. D. (2012). Agaricus subrufescens: a review. Saudi Journal of Biological Sciences, 19(2), 131-146.

Wu, J., Choi, J., Asiegbu, F. O., & Lee, Y. H. (2020). Comparative genomics platform and phylogenetic analysis of fungal laccases and multi-copper oxidases. Mycobiology, 48(5), 373-382.

Xiao, Y. Z., Chen, Q., Hang, J., Shi, Y. Y., Xiao, Y. Z., Wu, J., Hong, Y.Z., & Wang, Y. P. (2004). Selective induction, purification and characterization of a laccase isozyme from the basidiomycete Trametes sp. AH28-2. Mycologia, 96(1), 26-35.

Yan, L., Xu, R., Bian, Y., Li, H., & Zhou, Y. (2019). Expression Profile of laccase gene family in white-rot basidiomycete Lentinula edodes under different environmental stresses. Genes, 10(12), 1045.

Yang, Y., Wei, F., Zhuo, R., Fan, F., Liu, H., Zhang, C., Ma, L., Jiang, M., & Zhang, X. (2013). Enhancing the laccase production and laccase gene expression in the white-rot fungus Trametes velutina 5930 with great potential for biotechnological applications by different metal ions and aromatic compounds. PLoS One, 8(11), e79307.

Published

15/12/2020

How to Cite

SOUZA, G. P. N. de; HALABURA, M. I. W.; AVELINO, K. V.; COSTA, M. R. da; SANTANA, T. T.; KASSEM, A. S. S.; MARIM, R. A.; NUNES, M. G. I. F.; COLAUTO, G. A. L.; COLAUTO, N. B.; VALLE, J. S. do. Laccase of Agaricus subrufescens cultivated with sugarcane molasses promotes the decolorization of synthetic dyes. Research, Society and Development, [S. l.], v. 9, n. 12, p. e12391210942, 2020. DOI: 10.33448/rsd-v9i12.10942. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/10942. Acesso em: 16 nov. 2024.

Issue

Section

Agrarian and Biological Sciences