Degradation of a leather-dye by the combination of depolymerised wood-chip biochar adsorption and solid-state fermentation with Trametes villosa SCS-10

Abstract

Adsorption into biochar-derived materials and mycoremediation are promising technologies for removing dyes from solid and liquid matrices. This study presents a combined treatment with adsorption into wood-chip biochar and mycodegradation under solid-state fermentation by Trametes villosa for removing the leather-dye Acid Blue 161. In the first stage, untreated wood-chip biochar, NaOH–depolymerised biochar and KMnO₄–depolymerised biochar were assessed for their dye removal efficiency by adsorption. KMnO₄–depolymerised biochar exhibited the highest adsorption (85.1 ± 1.9%) after 24 h of contact. KMnO₄–depolymerisation modified some physical and chemical properties on the untreated wood-chip biochar, increasing the surface area (50.4 m² g^–1), pore size (1.9 nm), and presence of surface functional groups. Response surface methodology coupled with a Box–Behnken design was used to optimise the AB₁₆₁ adsorption into the KMnO₄–depolymerised biochar. The optimised conditions, pH 3.0, dye concentration 100 mg L^–1 and sorbent dosage 2 g L^–1, led to a higher dye removal efficiency by adsorption (91.9 ± 1.0%). In a second stage, the wood-chip biochar supplemented with nutrients (1% malt extract and 0.5% peptone) was employed as a solid matrix for growing T. villosa and regenerating the dye-saturated material. After 15 days, T. villosa was able to grow (86.8 ± 0.8%), exhibit laccase activity (621.9 ± 62.3 U L^–1), and biodegrade (91.4 ± 1.3%) the dye adsorbed into the KMnO₄–depolymerised biochar. Finally, the mycoregenerated biochar was reutilised in a new cycle of adsorption reaching 79.5 ± 2.0% of dye removal efficiency by adsorption. This study revealed the potential of the combined treatment and is an initial assessment for developing commercial alternatives for treating leather industry wastewaters.

Keywords

White-rot fungi / Mycoremediation / Solid-state fermentation / Adsorption and biodegradation / Biochar / Biomass / Leather-dyes

References

[1] Ahmed MJ, Okoye PU, Hummadi EH, Hameed BH. High-performance porous biochar from the pyrolysis of natural and renewable seaweed (Gelidiella acerosa) and its application for the adsorption of methylene blue. Bioresour Technol, 2019, 278: 159-164.

[2] Aksu Z, Tatlı AI, Tunç O. A comparative adsorption/biosorption study of Acid Blue 161: effect of temperature on equilibrium and kinetic parameters. Chem Eng J, 2008, 142: 23-39.

[3] Arora DS, Gill P. Comparison of two assay procedures for lignin peroxidase. Enzyme Microb Technol, 2001, 28: 602-605.

[4] Asgher M, NoreenBilal SM. Enhancing catalytic functionality of Trametes versicolor ibl-04 laccase by immobilization on chitosan microspheres. Chem Eng Res Des, 2017, 119: 1-11.

[5] Bankole PO, Adekunle AA, Govindwar SP. Biodegradation of a monochlorotriazine dye, Cibacron Brilliant Red 3b-a in solid state fermentation by wood-rot fungal consortium, Daldinia concentrica and Xylaria polymorpha: co-biomass decolorization of Cibacron Brilliant Red 3b-a dye. Int J Biol Macromol, 2018, 120: 19-27.

[6] Behl K, Sinha S, Sharma M, Singh R, Joshi M, . One-time cultivation of Chlorella pyrenoidosa in aqueous dye solution supplemented with biochar for microalgal growth, dye decolorization and lipid production. Chem Eng J, 2019, 364: 552-561.

[7] Bernardino CAR, Mahler CF, Veloso MCC, Romeiro GA. Preparation of biochar from sugarcane by-product filter mud by slow pyrolysis and its use like adsorbent. Waste Biomass Valor, 2017, 8: 2511-2521.

[8] Bharti V, Vikrant K, Goswami M, Tiwari H, Sonwani RK, . Biodegradation of Methylene Blue dye in a batch and continuous mode using biochar as packing media. Environ Res, 2019, 171: 356-364.

[9] Boakye P, Tran HN, Lee DS, Woo SH. Effect of water washing pretreatment on property and adsorption capacity of macroalgae-derived biochar. J Environ Manage, 2019, 233: 165-174.

[10] Böhmer U, Frömmel S, Bley T, Müller M, Frankenfeld K, . Solid-state fermentation of lignocellulosic materials for the production of enzymes by the white-rot fungus Trametes hirsuta in a modular bioreactor. Eng Life Sci, 2011, 11: 395-401.

[11] Bourbonnais R, Paice MG, Reid ID, Lanthier P, Yaguchi M. Lignin oxidation by laccase isozymes from Trametes versicolor and role of the mediator 2,2´-Azinobis(3-Ethylbenzthiazoline-6-Sulfonate) in kraft lignin depolymerization. Appl Environ Microbiol, 1995, 61: 1876-1880.

[12] Braghiroli FL, Bouafif H, Neculita CM, Koubaa A. Activated biochar as an effective sorbent for organic and inorganic contaminants in water. Water Air Soil Pollut, 2018, 229: 1-22.

[13] Chaukura N, Murimba EC, Gwenzi W. Synthesis, characterisation and Methyl Orange adsorption capacity of Ferric Oxide-biochar nano-composites derived from pulp and paper sludge. Appl Water Sci, 2017, 7: 2175-2186.

[14] Chen SH, Ting ASY. Biodecolorisation and biodegradation potential of recalcitrant triphenylmethane dyes by Coriolopsis sp. Isolated from compost. J Environ Manage, 2015, 150: 274-280.

[15] Chen Y, Lin Y, Ho S, Zhou Y, Ren N. Highly efficient adsorption of dyes by biochar derived from pigments-extracted macroalgae pyrolyzed at different temperature. Bioresour Technol, 2018, 259: 104-110.

[16] Copete-Pertuz LS, Chanaga X, Barriuso J, López-Lucendo MF, Martínez MJ, Camarero S. Identification and characterization of laccase-type multicopper oxidases involved in dye-decolorization by the fungus Leptosphaerulina sp. BMC Biotechnol, 2015, 15: 1-13.

[17] Copete-Pertuz LS, Alandete-Novoa F, Placido J, Correa-Londoño GA, Mora-Martinez AL. Enhancement of ligninolytic enzymes production and decolourising activity in Leptosphaerulina Sp. by co-cultivation with Trichoderma viride and Aspergillus terreus. Sci Total Environ, 2019, 646: 1536-1545.

[18] da Fontoura JT, Rolim GS, Mella B, Farenzena M, Gutterres M. Defatted microalgal biomass as biosorbent for the removal of acid Blue 161 dye from tannery effluent. J Environ Chem Eng, 2017, 5: 5076-5084.

[19] Daâssi D, Zouari-Mechichi H, Frikha F, Rodríguez-Couto S, Nasri M, . Sawdust waste as a low-cost support-substrate for laccases production and adsorbent for azo dyes decolorization. J Environ Health Sci Engineer, 2016, 14: 1.

[20] Dai Y, Zhang N, Xing C, Cui Q, Sun Q. The adsorption, regeneration and engineering applications of biochar for removal organic pollutants: a review. Chemosphere, 2019, 223: 12-27.

[21] Daneshvar E, Vazirzadeh A, Niazi A, Kousha M, Naushad M, Bhatnagar A. Desorption of Methylene Blue dye from brown macroalga: effects of operating parameters, isotherm study and kinetic modeling. J Clean Prod, 2017, 152: 443-453.

[22] Das R, Bandyopadhyay R, Pramanik P. Carbon quantum dots from natural resource: a review. Mater Today Chem, 2018, 8: 96-109.

[23] El-Naggar A, El-Naggar AH, Shaheen SM, Sarkar B, Chang SX, . Biochar composition-dependent impacts on soil nutrient release, carbon mineralization, and potential environmental risk: A review. J Environ Manage, 2019, 241: 458-467.

[24] Gomes CS, Piccin JS, Gutterres M. Optimising adsorption parameters in tannery dye-containing effluent treatment with leather shaving waste. Process Saf Environ Prot, 2016, 99: 98-106.

[25] Jaramillo AC, Cobas M, Hormaza A, Sanroman MA. Degradation of adsorbed azo dye by solid-state fermentation: Improvement of culture conditions, a kinetic study, and rotating drum bioreactor performance. Water Air Soil Pollut, 2017, 228: 205.

[26] JiangLinMbog BYJK. Biochar derived from swine manure digestate and applied on the removals of heavy metals and antibiotics. Bioresour Technol, 2018, 270: 603-611.

[27] Kalpana D, Velmurugan N, Shim JH, Oh BT, Senthil K, . Biodecolourisation and biodegradation of reactive Levafix Blue E-RA granulate dye by the white Rot fungus Irpex lacteus. J Environ Manage, 2012, 111: 142-149.

[28] Katheresan V, Kansedo J, Lau SJ. Efficiency of various recent wastewater dye removal methods: a review. J Environ Chem Eng, 2018, 6: 4676-4697.

[29] Kaushik P, Malik A. Fungal dye decolourisation: recent advances and future potential. Environ Int, 2009, 35: 127-141.

[30] Li HX, Zhang RJ, Tang L, Zhang JH, Mao ZG. In vivo and in vitro decolourisation of synthetic dyes by laccase from solid state fermentation with Trametes sp. SYBC-L4. Bioprocess Biosyst Eng, 2014, 37: 2597-2605.

[31] Lian F, Cui G, Liu Z, Duo L, Zhang G, Xing B. One-step synthesis of a novel n-doped microporous biochar derived from crop straws with high dye adsorption capacity. J Environ Manage, 2016, 176: 61-68.

[32] Mann J, Markham JL, Peiris P, Spooner-Hart RN, Holford P, . Use of olive mill wastewater as a suitable substrate for the production of laccase by Cerrena Consors. Int Biodeter Biodegr, 2015, 99: 138-145.

[33] Martinez MJ, Francisco RD, Guillen F, Martinez AT. Purification and catalytic properties of two manganese peroxidase isoenzymes from Pleurotus Eryngii. Eur J Biochem, 1996, 237: 424-432.

[34] Meili L, Lins PV, Zanta CL, Soletti JI, Ribeiro LM, . MgAl-LDH/biochar composites for Methylene Blue removal by adsorption. Appl Clay Sci, 2019, 168: 11-20.

[35] Mella B, Puchana-Rosero MJ, Costa DES, Gutterres M. Utilisation of tannery solid waste as an alternative biosorbent for acid dyes in wastewater treatment. J Mol Liq, 2017, 242: 137-145.

[36] Nautiyal P, Subramanian KA, Dastidar MG. Adsorptive removal of dye using biochar derived from residual algae after in situ transesterification: alternate use of waste of biodiesel industry. J Environ Manage, 2016, 182: 187-197.

[37] Oliveira FR, Patel AK, Jaisi DP, Adhikari S, Lu H, Khanal SK. Environmental application of biochar: Current status and perspectives. Bioresour Technol, 2017, 246: 110-122.

[38] Ortiz-Monsalve S, Dornelles J, Poll E, Ramirez-Castrillon M, Valente P, Gutteres M. Biodecolourisation and biodegradation of leather dyes by a native isolate of Trametes villosa. Process Saf Environ Prot, 2017, 109: 437-451.

[39] Ortiz-Monsalve S, Valente P, Poll E, Jaramillo-Garcia V, Pegas Henriques JA. Biodecolourization and biodetoxification of dye-containing wastewaters from leather dyeing by the native fungal strain Trametes villosa SCS-10. Biochem Eng J, 2019, 141: 19-28.

[40] Ozmen N, Yesilada O. Valorization and biodecolorisation of dye adsorbed on lignocellulosics using white rot fungi. BioResources, 2012, 7: 1656-1665.

[41] Pandi A, Kuppuswami GM, Ramudu KN, Palanivel S. A sustainable approach for degradation of leather dyes by a new fungal laccase. J Clean Prod, 2019, 211: 590-597.

[42] Park JH, Wang JJ, Meng Y, Wei Z, DeLaune RD, . Adsorption/desorption behavior of cationic and anionic dyes by biochars prepared at normal and high pyrolysis temperatures. Colloid Surf A, 2019, 572: 274-282.

[43] Placido J, Capareda S. Production of silicon compounds and fulvic acids from cotton wastes biochar using chemical depolymerization. Ind Crop Prod, 2015, 67: 270-280.

[44] Placido J, Bustamante-López S, Meissner KE, Kelly DE, Kelly SL. NanoRefinery of carbonaceous nanomaterials: Complementing dairy manure gasification and their applications in cellular imaging and heavy metal sensing. Sci Total Environ, 2019, 689: 10-20.

[45] Placido J, Bustamante-López S, Meissner KE, Kelly DE, Kelly SL. Comparative study of the characteristics and fluorescent properties of three different biochar derived carbonaceous nanomaterials for bioimaging and heavy metal ions sensing. Fuel Proces Technol, 2019, 196: 106-163.

[46] Placido J, Bustamante-López S, Meissner KE, Kelly DE, Kelly SL. Microalgae biochar-derived carbon dots and their application in heavy metal sensing in aqueous systems. Sci Total Environ, 2019, 656: 531-539.

[47] Puchana-Rosero MJ, Lima EC, Ortiz-Monsalve S, Mella B, Costa DES, Poll E, Gutterres M. Fungal biomass as biosorbent for the removal of Acid Blue 161 dye in aqueous solution. Environ Sci Pollut Res, 2017, 24: 4200-4209.

[48] Rivera-Hoyos CM, Morales-Álvarez ED, Poutou-Piñales RA, Pedroza-Rodríguez AM, Rodríguez-Vázquez R, . Fungal laccases. Fungal. Biol Rev, 2013, 27: 67-82.

[49] Rodríguez-Couto S, Osma JF, Toca-Herrera JL. Removal of synthetic dyes by an eco-friendly strategy. Eng Life Sci, 2009, 9: 116-123.

[50] Salvador F, Martin-Sanchez N, Sanchez-Hernandez R, Sanchez-Montero MJ, Izquierdo C. Regeneration of carbonaceous adsorbents. Part II: chemical, microbiological and vacuum regeneration. Micropor Mesopor Mat, 2015, 202: 277-296.

[51] Saroj S, Kumar K, Pareek N, Prasad R, Singh RP. Biodegradation of azo dyes Acid Red 183, Direct Blue 15 and Direct Red 75 by the isolate Penicillium oxalicum SAR-3. Chemosphere, 2014, 107(240–248): 2014.

[52] Sewu DD, Boakye P, Jung H, Woo SH. Highly efficient adsorption of cationic dye by biochar produced with Korean cabbage waste. Bioresour Technol, 2017, 224: 206-213.

[53] Singh B, Singh BP, Cowie AL. Characterisation and evaluation of biochars for their application as a soil amendment. Soil Research, 2010, 48: 516-525.

[54] Song Z, Lian F, Yu Z, Zhu L, Xing B, Qiu W. Synthesis and characterization of a novel mnox-loaded biochar and its adsorption properties for Cu²⁺ in aqueous solution. Chem Eng J, 2014, 242: 36-42.

[55] Sumalinog DAG, Capareda SC, de Luna MDG. Evaluation of the effectiveness and mechanisms of acetaminophen and Methylene Blue dye adsorption on activated biochar derived from municipal solid wastes. J Environ Manage, 2018, 210: 255-262.

[56] Sun QY, Hong YZ, Xiao YZ, Fang W, Fang J. Decolorisation of textile reactive dyes by the crude laccase produced from solid-state fermentation of agro-by-products. World J Microb Biot, 2009, 25: 1153-1160.

[57] Thomas L, Larroche C, Pandey A. Current developments in solid-state fermentation. Biochem Eng J, 2013, 81: 146-161.

[58] Thommes M, Katsumi K, Neimark AV, Olivier JP, Rodriguez-Reinoso F, . Physisorption of gases, with special reference to the evaluation of surface area and pore size distribution (IUPAC technical report). Pure Appl Chem, 2015, 87: 1051-1069.

[59] Tran HN, Lee CK, VuChao MTHP. Removal of copper, lead, Methylene Green 5, and Acid Red 1 by saccharide-derived spherical biochar prepared at low calcination temperatures: Adsorption kinetics, isotherms, and thermodynamics. Water Air Soil Pollut, 2017, 228: 401.

[60] Vikrant K, Giri BS, Raza N, Roy K, Kim K, Rai BN, Singh RS. Recent advancements in bioremediation of dye: current status and challenges. Bioresour Technol, 2018, 253: 355-367.

[61] Vyavahare DG, Gurav RG, Jadhav PP, Patil RR, Aware CB, Jadhav JP. Response surface methodology optimization for sorption of Malachite Green dye on sugarcane bagasse biochar and evaluating the residual dye for phyto and cytogenotoxicity. Chemosphere, 2018, 194: 306-315.

[62] Wang X, Bayan MR, Yu M, Ludlow DK, Liang X. Atomic layer deposition surface functionalized biochar for adsorption of organic pollutants: improved hydrophilia and adsorption capacity. Int J Environ Sci Technol, 2017, 14: 1825-1843.

[63] Wathukarage A, Herath I, Iqbal MCM, Vithanage M. Mechanistic understanding of crystal violet dye sorption by woody biochar: implications for wastewater treatment. Environ Geochem Health, 2017, 41: 1647-1661.

[64] Xu Y, Liu Y, Liu S, Tan X, Zeng G, . Enhanced adsorption of Methylene Blue by citric acid modification of biochar derived from water hyacinth (Eichornia crassipes). Environ Sci Pollut Res, 2016, 23: 23606-23618.

[65] Zazycki MA, Godinho M, Perondi D, Foletto EL, Collazzo GC, Dotto GL. New biochar from pecan nutshells as an alternative adsorbent for removing Reactive Red 141 from aqueous solutions. J Clean Prod, 2018, 171: 57-65.

[66] Zeng G, Cheng M, Huang D, Lai C, Xu P, Wei Z, Li N, Zhang C, He X, He Y. Study of the degradation of methylene blue by semi-solid-state fermentation of agricultural residues with Phanerochaete chrysosporium and reutilization of fermented residues. J Waste Manag, 2015, 38: 424-430.

[67] Zhu K, Wang X, Chen D, Ren W, Lin H. Wood-based biochar as an excellent activator of peroxydisulfate for Acid Orange 7 decolorization. Chemosphere, 2019, 231: 32-40.

Funding

European Regional Development Fund (ERDF)

Welsh European Funding Office (WEFO)

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior(PDSE)