Bioremediation and Detoxification of the Textile Dye Methyl Blue by Trichoderma asperellum LBKURCC1 with Laccase Activity

Andi Dahliaty; Yuana Nurulita; Ismawati; Nuria Wulandari; Dwi Kurniati; Yanti; Titania Tjandrawati Nugroho

doi:10.22146/jtbb.16121

Andi Dahliaty Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Riau, Kampus Bina Widya, Jl. Raya Soebrantas Km 12,5, Pekanbaru, Riau 28293, Indonesia https://orcid.org/0000-0002-5119-5333
Yuana Nurulita Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Riau, Kampus Bina Widya, Jl. Raya Soebrantas Km 12,5, Pekanbaru, Riau 28293, Indonesia https://orcid.org/0000-0001-5486-4048
Ismawati Faculty of Medicine, Universitas Riau, Jl. Diponegoro no. 1, Pekanbaru, Riau 28133, Indonesia https://orcid.org/0000-0003-0742-2719
Nuria Wulandari Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Riau, Kampus Bina Widya, Jl. Raya Soebrantas Km 12,5, Pekanbaru, Riau 28293, Indonesia https://orcid.org/0009-0004-1604-3715
Dwi Kurniati Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Riau, Kampus Bina Widya, Jl. Raya Soebrantas Km 12,5, Pekanbaru, Riau 28293, Indonesia https://orcid.org/0009-0005-9143-5062
Yanti Faculty of Biotechnology, Atma Jaya Catholic University of Indonesia, Kampus III BSD, Jl. Raya Cisauk, Tangerang, Banten 15345, Indonesia https://orcid.org/0000-0002-9330-5780
Titania Tjandrawati Nugroho Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Riau, Kampus Bina Widya, Jl. Raya Soebrantas Km 12,5, Pekanbaru, Riau 28293, Indonesia https://orcid.org/0000-0001-9825-7549

DOI: https://doi.org/10.22146/jtbb.16121

Keywords: Bioremediation, Laccase, Methyl blue, Trichoderma asperellum, Triphenylmethane

Abstract

Textile production generates effluent contaminated by 10-15 % dyes used. Fungal-mediated remediation presents an ecologically acceptable and inexpensive method for treating dye effluents. Trichoderma asperellum LBKURCC1 isolated from Riau cacao rhizosphere produces laccase. Laccase can catalyse the degradation of several textile dyes. This study aims to investigate T. asperellum LBKURCC1 ability to bioremediate and to detoxify the textile triphenylmethane dye, methyl blue (MB). T. asperellum LBKURCC1 cultures in minimal media with pHs of 4.5, 5.5 and 6.5 were incubated (24 hours, room temperature) with 50-ppm MB solutions. MB decolorisation analysis was conducted by examining the UV-Vis absorption spectra of MB after 24 hours treatment. It was also determined if the degradation was contributed by enzymatic biodegradation or by biosorption processes. The contribution of laccase activity to the bioremediation process was assessed by monitoring laccase activity in fungal treated MB solution. Acute toxicity of MB to Artemia salina larvae was determined pre- and post-fungal treatment. The results showed that decolorisation of MB by T. asperellum LBKURCC1 occurred at all tested pH levels, but at different rates for different pH. The highest decolorisation rate was at pH 4.5 (85 % per 24 hours). Enzymatic biodegradation was the higher contributor to the decolorisation, compared to mycelia biosorption. Laccase activity was induced by MB and the highest activity was found at pH 4.5. MB toxicity to A. salina larvae was eliminated by the fungal biodegradation. This study confirms the potential of T. asperellum LBKURCC1 life cultures in the degradation of MB, eliminating its toxicity.

References

Adenan, N.H., Lim, Y.Y. & Ting, A.S.Y., 2022. Removal of triphenylmethane dyes by Streptomyces bacillaris: A study on decolorization, enzymatic reactions and toxicity of treated dye solutions. Journal of Environmental Management, 318, 115520. doi: 10.1016/j.jenvman.2022.115520.

Adnan, L.A. et al., 2017. Rapid bioremediation of Alizarin Red S and Quinizarine Green SS dyes using Trichoderma lixii F21 mediated by biosorption and enzymatic processes. Bioprocess and Biosystems Engineering, 40(1), pp.85–97. doi: 10.1007/s00449-016-1677-7.

Al-Tohamy, R. et al., 2022. A critical review on the treatment of dye-containing wastewater: Ecotoxicological and health concerns of textile dyes and possible remediation approaches for environmental safety. Ecotoxicology and Environmental Safety, 231, 113160. doi: 10.1016/j.ecoenv.2021.113160.

Alam, R. et al., 2021. Biodegradation and metabolic pathway of anthraquinone dyes by Trametes hirsuta D7 immobilized in light expanded clay aggregate and cytotoxicity assessment. Journal of Hazardous Materials, 405, 124176. doi: 10.1016/j.jhazmat.2020.124176.

Ali, S.S. et al., 2022. Exploring the potential of a newly constructed manganese peroxidase-producing yeast consortium for tolerating lignin degradation inhibitors while simultaneously decolorizing and detoxifying textile azo dye wastewater. Bioresource Technology, 351, 126861. doi: 10.1016/j.biortech.2022.126861.

Anita, S.H. et al., 2022. Decolorization of Synthetic Dyes by Tropical Fungi Isolated from Taman Eden 100, Toba Samosir, North Sumatra, Indonesia. HAYATI Journal of Biosciences, 29(4), pp.417–427. doi: 10.4308/hjb.29.4.417-427.

Ardiati, F.C. et al., 2024. Evaluation of batch and fed-batch rotating drum biological contactor using immobilized Trametes hirsuta EDN082 for non-sterile real textile wastewater treatment. Journal of Environmental Chemical Engineering, 12(4), 113241. doi: 10.1016/j.jece.2024.113241.

Argumedo-Delira, R., Gómez-Martínez, M.J. & Uribe-Kaffure, R., 2021. Trichoderma biomass as an alternative for removal of congo red and malachite green industrial dyes. Applied Sciences (Switzerland), 11(1), 448. doi: 10.3390/app11010448.

Arora, S. et al., 2022. Innovations in Environmental Biotechnology, Singapore: Springer Singapore. doi: 10.1007/978-981-16-4445-0.

Arslantaş, C. et al., 2022. Basic Red 18 and Remazol Brilliant Blue R biosorption using Russula brevipes, Agaricus augustus, Fomes fomentarius. Water Practice and Technology, 17(3), pp.749–762. doi: 10.2166/wpt.2022.008.

Asses, N. et al., 2018. Congo Red Decolorization and Detoxification by Aspergillus niger : Removal Mechanisms and Dye Degradation Pathway. BioMed Research International, 2018, 3049686. doi: 10.1155/2018/3049686.

Barapatre, A., Aadil, K.R. & Jha, H., 2017. Biodegradation of Malachite Green by the Ligninolytic Fungus Aspergillus flavus. Clean - Soil, Air, Water, 45(4), 1600045. doi: 10.1002/clen.201600045.

Ben Ali, W. et al., 2020. Screening of five marine-derived fungal strains for their potential to produce oxidases with laccase activities suitable for biotechnological applications. BMC Biotechnology, 20(1), 27. doi: 10.1186/s12896-020-00617-y.

Bernats, M. & Juhna, T., 2018. Removal of phenols-like substances in pharmaceutical wastewater with fungal bioreactors by adding Trametes versicolor. Water Science and Technology, 78(4), pp.743–750. doi: 10.2166/wst.2018.340.

Boer, C.G. et al., 2004. Decolorization of synthetic dyes by solid state cultures of Lentinula (Lentinus) edodes producing manganese peroxidase as the main ligninolytic enzyme. Bioresource Technology, 94(2), pp.107–112. doi: 10.1016/j.biortech.2003.12.015.

Carballo, J.L. et al., 2002. A comparison between two brine shrimp assays to detect in vitro cytotoxicity in marine natural products. BMC Biotechnology, 2, 17. doi: 10.1186/1472-6570-2-17

Chatha, S.A.S., Asgher, M. & Iqbal, H.M.N., 2017. Enzyme-based solutions for the textile processing and dye contaminant biodegradation-a review. Environmental Science and Pollution Research, 24, pp.14005–14018. doi: 10.1007/s11356-017-8998-1.

Couto, S.R., 2009. Dye Removal by Immobilized Fungi. Biotechnology Advances, 27(3), pp.227–235. doi: 10.1016/j.biotechadv.2008.12.001.

Dahlena, M. et al., 2022. Preliminary kinetic studies on the degradation of the textile dye methyl blue by Trichoderma asperellum LBKURCC1 laccase without mediators. AIP Conference Proceedings, 2638, 100005. doi: 10.1063/5.0104615.

Drăgoi, M. et al., 2021. Degradation of Methyl Blue By Fenton Process. Annals of the University of Craiova, Series Chemistry, 27(2), pp.53–59. doi: 10.52846/aucchem.2021.2.06.

Eteba, A., Bassyouni, M. & Saleh, M., 2023. Utilization of chemically modified coal fly ash as cost-effective adsorbent for removal of hazardous organic wastes. International Journal of Environmental Science and Technology, 20(7), pp.7589–7602. doi: 10.1007/s13762-022-04457-5.

Ghosh, A., Dastidar, M.G. & Sreekrishnan, T.R., 2017. Response surface modeling of bioremediation of acid black 52 dye using Aspergillus flavus. Water Science and Technology, 75(12), pp.2864–2874. doi: 10.2166/wst.2017.167.

He, X. ling et al., 2018. Efficient degradation of Azo dyes by a newly isolated fungus Trichoderma tomentosum under non-sterile conditions. Ecotoxicology and Environmental Safety, 150, pp.232–239. doi: 10.1016/j.ecoenv.2017.12.043.

Jeon, S.-J. & Lim, S.-J., 2017. Purification and Characterization of the Laccase Involved in Dye Decolorization by the White-Rot Fungus Marasmius scorodonius. Journal of Microbiology and Biotechnology, 27, pp.1120–1127. doi: 10.4014/jmb.1701.01004

Juárez-Hernández, J. et al., 2021. Isolation of Fungi from a Textile Industry Effluent and the Screening of Their Potential to Degrade Industrial Dyes. Journal of Fungi, 7, 805. doi: 10.3390/jof7100805.

Kumar, A. & Arora, P.K., 2022. Biotechnological Applications of Manganese Peroxidases for Sustainable Management. Frontiers in Environmental Science, 10, 875157. doi: 10.3389/fenvs.2022.875157.

Kumar, A., Kumar, S. & Ratna, S., 2024. Nature-Based Wastewater Treatment Systems:Emerging Approaches with Potential Resource Recovery Options, Boca Raton: CRC Press. doi: 10.1201/9781003441144.

Lanfranconi, I. et al., 2022. Textile dyeing wastewater treatment by Penicillium chrysogenum: Design of a sustainable process. Water Science and Technology, 86(2), pp.292–301. doi: 10.2166/wst.2022.204.

Latha, L.Y. et al., 2007. Antibacterial activity and toxicity of Psophocarpus tetragonolobus. Pharmaceutical Biology, 45(1), pp.31–36. doi: 10.1080/13880200601026317.

Mohammed, Y.M.M. & Mabrouk, M.E.M., 2020. Optimization of methylene blue degradation by Aspergillus terreus YESM 3 using response surface methodology. Water Science and Technology, 82(10), pp.2007–2018. doi: 10.2166/wst.2020.476.

Morshed, M.H. et al., 2018. Cytotoxicity of Four Active Dyes Against Artemia salina Leach. Journal of Engineering Science, 9(2), pp.55–59.

Munck, C. et al., 2018. Biofilm formation of filamentous fungi Coriolopsis sp. on simple muslin cloth to enhance removal of triphenylmethane dyes. Journal of Environmental Management, 214, pp.261–266. doi: 10.1016/j.jenvman.2018.03.025.

Mutambyi, V. et al., 2023. Removal of Reactive Black 5 from simulated textile effluents by an electrocoagulation process: optimization by response surface methodology. Water Practice and Technology, 18(12), pp.3048–3064. doi: 10.2166/wpt.2023.210.

Nadew, T.T. et al., 2023. Synthesis of activated carbon from banana peels for dye removal of an aqueous solution in textile industries: optimization, kinetics, and isotherm aspects. Water Practice and Technology, 18(4), pp.947–966. doi: 10.2166/wpt.2023.042.

Nugroho, T.T. et al., 2023. Bioremediation , Biosorption , and Biodegradation of the Textile Dye Reactive Black 5 by Life Cultures of Trichoderma asperellum. Jurnal Natur Indonesia, 21(2), pp.93–99. doi: 10.31258/jnat.21.2.93-99.

Nugroho, T.T. et al., 2018. Colour removal of an azo-textile dye and production of laccase by submerged cultures of Trichoderma asperellum LBKURCC1. Journal of Physics: Conference Series, 1116(4), 042027. doi: 10.1088/1742-6596/1116/4/042027.

Pedroza, A.M. et al., 2007. Sequential treatment via Trametes versicolor and UV/TiO2/RuxSey to reduce contaminants in waste water resulting from the bleaching process during paper production. Chemosphere, 67(4), pp.793–801. doi: 10.1016/j.chemosphere.2006.10.015.

Pereira, J.C.V., Serbent, M.P. & Skoronski, E., 2021. Application of immobilized mycelium-based pellets for the removal of organochlorine compounds: A review. Water Science and Technology, 83(8), pp.1781–1796. doi: 10.2166/wst.2021.093.

Plácido, J. et al., 2016. Degradation and detoxification of synthetic dyes and textile industry effluents by newly isolated Leptosphaerulina sp. from Colombia. Bioresources and Bioprocessing, 3, 6. doi: 10.1186/s40643-016-0084-x.

Procópio, A.M. da S. et al., 2023. Removal of 17α-ethinylestradiol (EE2) from aqueous solutions by peanut shells (Arachis hypogaea): adsorption kinetic, isothermal, and thermodynamic studies. Water Practice and Technology, 18(11), pp.2543–2560. doi: 10.2166/wpt.2023.183.

Rahayu, A.G. et al., 2019. Surfactant , Nitrogen and Carbon Media Optimization for Trichoderma asperellum LBKURCC1 Laccase Production by Flask Solid State Fermentation of Rice Straw. Journal of Physics: Conference Series, 1351, 012030. doi: 10.1088/1742-6596/1351/1/012030

Sandani, Y. et al., 2021. The effect of hydrogen peroxide on catalytic activity of manganosite MnO/ oil palm fly ash catalyst for degradation methylene blue. Journal of Physics: Conference Series, 2049(1), 012038. doi: 10.1088/1742-6596/2049/1/012038.

Sani, Z., Abdullahi, I. & Sani, A., 2018. Toxicity Evaluation of Selected Dyes Commonly used for Clothing Materials in Urban Kano, Nigeria. European Journal of Experimental Biology, 8(4), 26. doi: 10.21767/2248-9215.100067.

Sar, T. et al., 2024. Resource recovery and treatment of wastewaters using filamentous fungi. Science of the Total Environment, 951, 175752. doi: 10.1016/j.scitotenv.2024.175752.

Saravanakumar, K. & Kathiresan, K., 2014. Bioremoval of the synthetic dye malachite green by marine Trichoderma sp. Springer Plus, 3, 631. doi: 10.1186/2193-1801-3-631.

Sawitri, N., 2010. Penentuan beberapa parameter produksi kitinase Trichoderma asperellum T.N.C52 dan T.N.J63 pada berbagai substrat kitin. Universitas Riau.

Sellyna, N. et al., 2020. Optimalisasi waktu fermentasi, kadar air dan konsentrasi Cu2+ pada produksi lakase Trichoderma asperellum LBKURCC1 secara fermentasi padat batang padi dalam reaktor labu. Chimica et Natura Acta, 8, pp.7–16. doi: 10.24198/cna.v8.n1.26730.

Shanmugam, S. et al., 2017. Trichoderma asperellum laccase mediated crystal violet degradation-Optimization of experimental conditions and characterization. Journal of Environmental Chemical Engineering, 5(1), pp.222–231. doi: 10.1016/j.jece.2016.11.044.

Sing, N.N. et al., 2017. Decolourisation Capabilities of Ligninolytic Enzymes Produced by Marasmius cladophyllus UMAS MS8 on Remazol Brilliant Blue R and Other Azo Dyes. BioMed Research International, 2017, 1325754. doi: 10.1155/2017/1325754.

Singh, A.K. et al., 2021. Lignin peroxidase in focus for catalytic elimination of contaminants — A critical review on recent progress and perspectives. International Journal of Biological Macromolecules, 177, pp.58–82. doi: 10.1016/j.ijbiomac.2021.02.032.

Singh, N.J. et al., 2020. Alkali-cation-incorporated and functionalized iron oxide nanoparticles for methyl blue removal/decomposition. Nanotechnology, 31, 425703. doi: 10.1088/1361-6528/ab9af1.

Sinha, S. & Hanamghar, M., 2019. Acute Toxicity Of Triarylmethane Dye, Crystal Violet To Indian Major Carpfish, Labeo rohita. International Journal of Research and Analytical Reviews, 6(2), pp.288–300.

Siraj, Z. et al., 2021. KIT-6 induced mesostructured TiO2 for photocatalytic degradation of methyl blue. Environmental Science and Pollution Research, 28(38), pp.53340–53352. doi: 10.1007/s11356-021-14442-z.

Taharchaouche, D. et al., 2023. Degradation by hydrolysis of three triphenylmethane dyes: DFT and TD-DFT study. Theoretical Chemistry Accounts, 142(1), 10. doi: 10.1007/s00214-022-02950-1.

Tang, K.H.D. et al., 2022. Biological Removal of Dyes from Wastewater: A Review of Its Efficiency and Advances. Tropical Aquatic and Soil Pollution, 2(1), pp.59–75. doi: 10.53623/tasp.v2i1.72.

Wang, W. & Subramani, S., 2017. Assays to Monitor Pexophagy in Yeast. In Methods in Enzymology. Academic Press Inc., pp. 413–427. doi: 10.1016/bs.mie.2016.09.088.