La lacasa de Agaricus subrufescens cultivada en medio con melaza de caña de azúcar promueve la decoloración de tintes sintéticos
DOI:
https://doi.org/10.33448/rsd-v9i12.10942Palabras clave:
Agaricus blazei; Basidiomycota; Biodegradación; Colorantes textiles; Residuos agroindustriales.Resumen
Agaricus subrufescens es un hongo que produce lacasas, oxidorreductasas que degradan los colorantes. Las condiciones de cultivo como la concentración de nitrógeno, la fuente de carbono y los inductores pueden aumentar la producción de lacasa. El objetivo de este estudio fue cultivar A. subrufescens con urea, subproductos agroindustriales e inductores para producir lacasas para la decoloración de colorantes. Agaricus subrufescens U7-1 y U7-3 se cultivaron en medio líquido con urea (0, 2, 4, 6 y 8 g L-1), fuentes de carbono (glucosa, melaza de caña de azúcar - MC y melaza de soja - MS) e inductores (alcohol veratril, etanol, guayacol y vainillina). El extracto enzimático del cultivo se utilizó en la decoloración de remazol azul brillante R (RBBR), negro reactivo 5 (PR5) y verde malaquita (VM). La producción de lacasa de A. subrufescens fue inversamente proporcional a la concentración de urea y la mayor actividad lacasa de U7-1 ocurrió con 2 g L-1 de urea y U7-3 sin urea. MC aumentó la actividad y anticipó el pico de lacasa de U7-1 en cinco días y U7-3 en 15 días. MS redujo la actividad de lacasa. La vainillina aumentó la actividad lacasa de U7-1 en un 29% (44380 U L-1) y anticipó la actividad máxima; y la vainillina y el alcohol veratrílico aumentaron la actividad de lacasa de U7-3 (44770 U L-1), pero retrasaron la actividad máxima. Los extractos de U7-1 y U7-3 del cultivo de vainillina decoloraron el RBBR en 24 horas (65% y 75%) y VM (70%, 24 y 72 horas), pero no decoloraron PR5.
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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.
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Derechos de autor 2020 Genyfer Poline Neri de Souza; Marisangela Isabel Wietzikoski Halabura; Katielle Vieira Avelino; Marcella Ribeiro da Costa; Thiago Teodoro Santana; Adma Soraia Serea Kassem; Renan Alberto Marim; Maria Graciela Iecher Faria Nunes; Giani Andrea Linde Colauto; Nelson Barros Colauto; Juliana Silveira do Valle
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