Abstract
Laccases are versatile biocatalysts that are prominent for industrial purposes due to their extensive substrate specificity. Therefore, this research investigated producing laccase from Physisporinus vitreus via liquid fermentation. The results revealed that veratryl alcohol (4mM) was the most effective inducer 7500U/L. On the other hand, Zn ions inhibited laccase production. The optimum carbon and nitrogen sources were glucose and tryptone by 5200 and 3300 U/L, respectively. Moreover, solvents exhibited various impacts on the enzyme activity at three different solvent concentrations (5%, 10% and 20%), however, it showed a highest activity at 5% of the investigated solvent. Ferric ions inhibited the enzyme activity. In addition, the enzyme has a high ability to decolorize azo dyes when using syringaldehyde as a mediator. The purified laccase from Physisporinus vitreus is a promising substance to be used for industrial and environmental applications due to its stability under harsh conditions and efficiency in decolorization of dyes.
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Agustin MB, de Carvalho DM, Lahtinen MH, Hilden K, Lundell T, Mikkonen KS (2021) Laccase as a tool in building advanced lignin-based materials. Chemsuschem 14(21):4615–4635
Ajaz M, Shakeel S, Rehman A (2020) Microbial use for azo dye degradation—a strategy for dye bioremediation. Int Microbiol 23:149–159
Alhujaily A, Yu H, Zhang X, Ma F (2020) Adsorptive removal of anionic dyes from aqueous solutions using spent mushroom waste. Appl Water Sci 10(7):183. https://doi.org/10.1007/s13201-020-01268-2
Arregui L, Ayala M, Gómez-Gil X, Gutiérrez-Soto G, Hernández-Luna CE, de Los H, Santos M, Levin L, Rojo-Domínguez A, Romero-Martínez D, Saparrat MCN, Trujillo-Roldán MA, Valdez-Cruz NA (2019) Laccases: structure, function, and potential application in water bioremediation. Microb Cell Fact 18(1):200. https://doi.org/10.1186/s12934-019-1248-0
Bankole PO, Omoni VT, Tennison-Omovoh CA, Adebajo SO, Mulla SI, Adekunle AA, Semple KT (2022) Novel laccase from Xylaria polymorpha and its efficiency in the biotransformation of pharmaceuticals: Optimization of operational conditions, comparative effect of redox-mediators and toxicity studies. Colloids Surf, B 217:112675
Barh A, Sharma K, Bhatt P, Annepu SK, Nath M, Shirur M, Kumari B, Kaundal K, Kamal S, Sharma VP (2022) Identification of key regulatory pathways of basidiocarp formation in Pleurotus spp. using modeling, simulation and system biology studies. J Fungi 8(10):1073
Bhuvaneswari, M., Subashini, R., Crossia, J. W. F., & Vijayalakshmi, S. (2020). Mycoremediation of industrial dyes by laccases. In New and Future Developments in Microbial Biotechnology and Bioengineering (pp. 235–243). Elsevier.
Bonugli-Santos RC, Durrant LR, da Silva M, Sette LD (2010) Production of laccase, manganese peroxidase and lignin peroxidase by Brazilian marine-derived fungi. Enzyme Microbial Technol 46(1):32–37
Burton SG (2003) Laccases and phenol oxidases in organic synthesis-a review. Curr Org Chem 7(13):1317–1331
Camarero S, Ibarra D, Martínez MJ, Martínez ÁT (2005) Lignin-derived compounds as efficient laccase mediators for decolorization of different types of recalcitrant dyes. Appl Env Microbiol 71(4):1775–1784
Cañas AI, Camarero S (2010) Laccases and their natural mediators: biotechnological tools for sustainable eco-friendly processes. Biotechnol Adv 28(6):694–705
Cardullo N, Muccilli V, Tringali C (2022) Laccase-mediated synthesis of bioactive natural products and their analogues. RSC Chemical Biology 3(6):614–647
Chan Cupul W, Heredia Abarca G, Martínez Carrera D, Rodríguez Vázquez R (2014) Enhancement of ligninolytic enzyme activities in a Trametes maxima–Paecilomyces carneus co-culture: Key factors revealed after screening using a Plackett-Burman experimental design. Electron J Biotechnol 17(3):114–121
Chen L, Zhang X, Zhang M, Zhu Y, Zhuo R (2022) Removal of heavy-metal pollutants by white rot fungi: Mechanisms, achievements, and perspectives. J Clean Prod 354:131681
Chen S, Zhu M, Guo X, Yang B, Zhuo R (2023) Coupling of Fenton reaction and white rot fungi for the degradation of organic pollutants. Ecotoxicol Environ Saf 254:114697. https://doi.org/10.1016/j.ecoenv.2023.114697
Chmelová D, Legerská B, Kunstová J, Ondrejovič M, Miertuš S (2022) The production of laccases by white-rot fungi under solid-state fermentation conditions. World J Microbiol Biotechnol 38(2):21. https://doi.org/10.1007/s11274-021-03207-y
Dhaarani S, Priya AK, Rajan TV, Kartic DN (2012) Degradation of various dyes using Laccase enzyme. J Environ Sci Eng 54(4):489–494
Durán-Sequeda D, Suspes D, Maestre E, Alfaro M, Perez G, Ramírez L, Pisabarro AG, Sierra R (2022) Effect of nutritional factors and copper on the regulation of laccase enzyme production in Pleurotus ostreatus. J Fungi 8(1):7
Dwivedi, U. N., Singh, P., Pandey, V. P., & Kumar, A. (2011). Structure–function relationship among bacterial, fungal and plant laccases. Journal of Molecular Catalysis B: Enzymatic, 68(2), 117–128. http://ac.els-cdn.com/S1381117710002857/1-s2.0-S1381117710002857-main.pdf?_tid=02f61d9e-d4d2-11e3-82b6-00000aacb360&acdnat=1399348601_f68b8f633bb0d3d38208847a518a88fd
Elfarash A, Mawad AMM, Yousef NMM, Shoreit AAM (2017) Azoreductase kinetics and gene expression in the synthetic dyes-degrading Pseudomonas. Egypt J Basic Appl Sci 4(4):315–322
Ellouze, M., & Sayadi, S. (2016). White-rot fungi and their enzymes as a biotechnological tool for xenobiotic bioremediation. Management of hazardous wastes, 103–120.
Forootanfar H, Faramarzi MA, Shahverdi AR, Yazdi MT (2011) Purification and biochemical characterization of extracellular laccase from the ascomycete Paraconiothyrium variabile. Bioresour Technol 102(2):1808–1814. https://doi.org/10.1016/j.biortech.2010.09.043
Fürtges L, Obermaier S, Thiele W, Foegen S, Müller M (2019) Diversity in fungal intermolecular phenol coupling of polyketides: Regioselective laccase-based systems. ChemBioChem 20(15):1928–1932
Gałązka A, Jankiewicz U (2022) Endocrine disrupting compounds (nonylphenol and bisphenol A)–sources, harmfulness and laccase-assisted degradation in the aquatic environment. Microorganisms 10(11):2236
Galhaup C, Wagner H, Hinterstoisser B, Haltrich D (2002) Increased production of laccase by the wood-degrading basidiomycete< i> Trametes pubescens</i>. Enzyme Microb Technol 30(4):529–536
Gao X, Wei M, Zhang X, Xun Y, Duan M, Yang Z, Zhu M, Zhu Y, Zhuo R (2024) Copper removal from aqueous solutions by white rot fungus Pleurotus ostreatus GEMB-PO1 and its potential in co-remediation of copper and organic pollutants. Biores Technol 395:130337
Souza GMD, C., Kirst Tychanowicz, G., Farani De Souza, D., & Peralta, R. M. (2004) Production of laccase isoforms by Pleurotus pulmonarius in response to presence of phenolic and aromatic compounds. J Basic Microbiol 44(2):129–136
Gnanamani A, Jayaprakashvel M, Arulmani M, Sadulla S (2006) Effect of inducers and culturing processes on laccase synthesis in Phanerochaete chrysosporium NCIM 1197 and the constitutive expression of laccase isozymes. Enzyme Microbial Technol 38(7):1017–1021
Gomez-Fernandez BJ, Risso VA, Sanchez-Ruiz JM, Alcalde M (2020) Consensus design of an evolved high-redox potential laccase. Frontiers in Bioengineering and Biotechnology 8:354
He X-L, Song C, Li Y-Y, Wang N, Xu L, Han X, Wei D-S (2018) Efficient degradation of Azo dyes by a newly isolated fungus Trichoderma tomentosum under non-sterile conditions. Ecotoxicol Environ Saf 150:232–239
Hildén K, Hakala TK, Maijala P, Lundell TK, Hatakka A (2007) Novel thermotolerant laccases produced by the white-rot fungus Physisporinus rivulosus. Appl Microbiol Biotechnol 77(2):301–309. https://doi.org/10.1007/s00253-007-1155-x
Imran M, Asad MJ, Hadri SH, Mehmood S (2012) Production and industrial applications of laccase enzyme. Journal of Cell and Molecular Biology 10(1):1
Kaal EE, Field JA, Joyce TW (1995) Increasing ligninolytic enzyme activities in several white-rot basidiomycetes by nitrogen-sufficient media. Biores Technol 53(2):133–139
Kong W, Fu X, Wang L, Alhujaily A, Zhang J, Ma F, Zhang X, Yu H (2017) A novel and efficient fungal delignification strategy based on versatile peroxidase for lignocellulose bioconversion. Biotechnol Biofuels 10:218. https://doi.org/10.1186/s13068-017-0906-x
Kumar VV, Sathyaselvabala V, Premkumar MP, Vidyadevi T, Sivanesan S (2012) Biochemical characterization of three phase partitioned laccase and its application in decolorization and degradation of synthetic dyes. J Molr Cataly B 74(1):63–72
Kunamneni A, Ballesteros A, Plou FJ, Alcalde M (2007) Fungal laccase—a versatile enzyme for biotechnological applications. Communicating Current Research and Educational Topics and Trends in Applied Microbiology 1:233–245
Lee I-Y, Jung K-H, Lee C-H, Park Y-H (1999) Enhanced production of laccase in Trametes vesicolor by the addition of ethanol. Biotechnol Lett 21(11):965–968
Lin S, Wei J, Yang B, Zhang M, Zhuo R (2022) Bioremediation of organic pollutants by white rot fungal cytochrome P450: The role and mechanism of CYP450 in biodegradation. Chemosphere 301:134776
Liu X, Deng W, Yang Y (2021) Characterization of a novel Laccase LAC-Yang1 from White-Rot fungus Pleurotus ostreatus strain Yang1 with a strong ability to degrade and detoxify chlorophenols. Molecules 26(2):473
Lucas MS, Peres JA (2006) Decolorization of the azo dye Reactive Black 5 by Fenton and photo-Fenton oxidation. Dyes Pigm 71(3):236–244
Mawad AMM, Yousef NMH, Shoreit AAM (2016) Robust Aspergillus terreus biofilm supported on graphene oxide/hematite-nanocomposites for adsorption of anthraquinone dye. Desalin Water Treat 57(51):24341–24351. https://doi.org/10.1080/19443994.2016.1138885
Mawad AM, Abd Hesham E-L, Yousef NM, Shoreit AA, Gathergood N, Gupta VK (2020a) Role of bacterial-fungal consortium for enhancement in the degradation of industrial dyes. Curr Genomics 21(4):283–294
Mawad, A. M. M., Hesham, A. E.-L., Khan, S., & Nawab, J. (2020b). The Role of Fungi and Genes for the Removal of Environmental Contaminants from Water/Wastewater Treatment Plants. In A. E.-L. Hesham, R. S. Upadhyay, G. D. Sharma, C. Manoharachary, & V. K. Gupta (Eds.), Fungal Biotechnology and Bioengineering (pp. 349–370). Springer International Publishing. https://doi.org/10.1007/978-3-030-41870-0_15
Mayer AM, Staples RC (2002) Laccase: new functions for an old enzyme. Phytochemistry 60(6):551–565
Mendoza L, Jonstrup M, Hatti-Kaul R, Mattiasson B (2011) Azo dye decolorization by a laccase/mediator system in a membrane reactor: Enzyme and mediator reusability. Enzyme Microbial Technol 49(5):478–484
Mónica M-GA, Jaime MQ (2019) Phenoloxidases of fungi and bioremediation. Fungal Bioremediation Fundam Appl 3:62–90
More, S. S., PS, R., Malini, S., & SM, V. (2011). Isolation, purification, and characterization of fungal laccase from Pleurotus sp. Enzyme research, 2011.
Murugesan K, Arulmani M, Nam I-H, Kim Y-M, Chang Y-S, Kalaichelvan PT (2006) Purification and characterization of laccase produced by a white rot fungus Pleurotus sajor-caju under submerged culture condition and its potential in decolorization of azo dyes. Appl Microbiol Biotechnol 72(5):939–946
Murugesan K, Kim Y-M, Jeon J-R, Chang Y-S (2009) Effect of metal ions on reactive dye decolorization by laccase from Ganoderma lucidum. J Hazard Mater 168(1):523–529
Nahas, H. H. A., Mansour, S. A., Nouh, F. A. A., Landa-Acuña, D., Nahas, Y. H. A., Nieto-Taype, M. A., & Abdel-Azeem, A. M. (2021). Fungal Laccases to Where and Where? Industrially Important Fungi for Sustainable Development: Volume 2: Bioprospecting for Biomolecules, 205.
Pandey A, Singh P, Iyengar L (2007) Bacterial decolorization and degradation of azo dyes. Int Biodeterior Biodegradation 59(2):73–84
Park S, Jung D, Do H, Yun J, Lee D, Hwang S, Lee SH (2021) Laccase-mediator system using a natural mediator as a whitening agent for the decolorization of melanin. Polymers 13(21):3671
Penttilä, R., & Kotiranta, H. (1996). Short-term effects of prescribed burning on wood-rotting fungi.
Peterson GL (1977) A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem 83(2):346–356
Rathi BS, Kumar PS (2022) Sustainable approach on the biodegradation of azo dyes: a short review. Current Opinion in Green and Sustainable Chemistry 33:100578
Revankar MS, Lele S (2006) Enhanced production of laccase using a new isolate of white rot fungus< i> WR-1</i>. Process Biochem 41(3):581–588
Riegas-Villalobos A, Martínez-Morales F, Tinoco-Valencia R, Serrano-Carreón L, Bertrand B, Trejo-Hernández MR (2020) Efficient removal of azo-dye Orange II by fungal biomass absorption and laccase enzymatic treatment. 3 Biotech 10:1–10
Riva S (2006) Laccases: blue enzymes for green chemistry. TRENDS in Biotechnol 24(5):219–226
Rodakiewicz-Nowak J, Kasture S, Dudek B, Haber J (2000) Effect of various water-miscible solvents on enzymatic activity of fungal laccases. J Mol Catal B Enzym 11(1):1–11
Sadhasivam S, Savitha S, Swaminathan K, Lin F-H (2008) Production, purification and characterization of mid-redox potential laccase from a newly isolated Trichoderma harzianum WL1. Process Biochem 43(7):736–742
Si J, Peng F, Cui B (2013) Purification, biochemical characterization and dye decolorization capacity of an alkali-resistant and metal-tolerant laccase from Trametes pubescens. Biores Technol 128:49–57
Singh, G., Dwivedi, S. K., & Mishra, J. (2020). Role of Fungal Enzymes in the Removal of Azo Dyes. In N. K. Arora, J. Mishra, & V. Mishra (Eds.), Microbial Enzymes: Roles and Applications in Industries (pp. 231–257). Springer Singapore. https://doi.org/10.1007/978-981-15-1710-5_9
Srinivasulu C, Ramgopal M, Ramanjaneyulu G, Anuradha CM, Suresh Kumar C (2018) Syringic acid (SA) - A Review of Its Occurrence, Biosynthesis, Pharmacological and Industrial Importance. Biomed Pharmacother 108:547–557. https://doi.org/10.1016/j.biopha.2018.09.069
Sun J, Chen Q-J, Zhu M-J, Wang H-X, Zhang G-Q (2014) An extracellular laccase with antiproliferative activity from the sanghuang mushroom Inonotus baumii. J Mol Catal B Enzym 99:20–25
Sun Y, Liu Z-L, Hu B-Y, Chen Q-J, Yang A-Z, Wang Q-Y, Li X-F, Zhang J-Y, Zhang G-Q, Zhao Y-C (2021) Purification and characterization of a thermo-and pH-stable laccase from the litter-decomposing fungus Gymnopus luxurians and laccase mediator systems for dye decolorization. Front Microbiol 12:672620
Thapa S, Li H, OHair, J., Bhatti, S., Chen, F.-C., Nasr, K. A., Johnson, T., & Zhou, S. (2019) Biochemical characteristics of microbial enzymes and their significance from industrial perspectives. Mol Biotechnol 61:579–601
Unuofin JO, Moloantoa KM, Khetsha ZP (2022) The biobleaching potential of laccase produced from mandarin peelings: Impetus for a circular bio-based economy in textile biofinishing. Arab J Chem 15(12):104305
Vantamuri AB, Kaliwal BB (2016) Purification and characterization of laccase from Marasmius species BBKAV79 and effective decolorization of selected textile dyes. 3 Biotech 6(2):189
Wan Y-Y, Lu R, Xiao L, Du Y-M, Miyakoshi T, Chen C-L, Knill CJ, Kennedy JF (2010) Effects of organic solvents on the activity of free and immobilised laccase from Rhus vernicifera. Int J Biol Macromol 47(4):488–495
Wang S-N, Chen Q-J, Zhu M-J, Xue F-Y, Li W-C, Zhao T-J, Li G-D, Zhang G-Q (2018) An extracellular yellow laccase from white rot fungus Trametes sp. F1635 and its mediator systems for dye decolorization. Biochimie 148:46–54
Xiao Y, Chen Q, Hang J, Shi Y, Wu J, Hong Y, Wang Y (2004) Selective induction, purification and characterization of a laccase isozyme from the basidiomycete Trametes sp. AH28–2. Mycologia 96(1):26–35
Yang Y, Ding Y, Liao X, Cai Y (2013) Purification and characterization of a new laccase fromShiraia sp SUPER-H168. Process Biochem 48(2):351–357
Younes SB, Sayadi S (2011) Purification and characterization of a novel trimeric and thermotolerant laccase produced from the ascomycete Scytalidium thermophilum strain. J Mol Catal B Enzym 73(1–4):35–42
Zhang J, Ke W, Chen H (2020) Enhancing laccase production by white-rot fungus Trametes hirsuta SSM-3 in co-culture with yeast sporidiobolus pararoseus SSM-8. Prep Biochem Biotechnol 50(1):10–17
Zhuo R, Fan F (2021) A comprehensive insight into the application of white rot fungi and their lignocellulolytic enzymes in the removal of organic pollutants. Sci Total Env 778:146
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The author thanks the Key Laboratory of Molecular Biophysics of MOE, College of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, China.
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AA performed the methodology, wrote the first draft and drew the figures and tables. AMMM edited and finalized the last version of the manuscript, HMA performed data analysis and curation. MF did supervision and conceptualization. All authors reviewed the final version of the manuscript.
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Alhujaily, A., Mawad, A.M.M., Albasri, H.M. et al. Efficiency of thermostable purified laccase isolated from Physisporinus vitreus for azo dyes decolorization. World J Microbiol Biotechnol 40, 138 (2024). https://doi.org/10.1007/s11274-024-03953-9
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DOI: https://doi.org/10.1007/s11274-024-03953-9