Immobilization of laccase on organic–inorganic nanocomposites and its application in the removal of phenolic pollutants

Abstract

Polydopamine-functionalized nanosilica was synthesized using an inexpensive and easily obtainable raw material, mild reaction conditions, and simple operation. Subsequently, a flexible spacer arm was introduced by using dialdehyde starch as a cross-linking agent to bind with laccase. A high loading amount (77.8 mg∙g^‒1) and activity retention (75.5%) could be achieved under the optimum immobilization conditions. Thermodynamic parameters showed that the immobilized laccase had a lower thermal deactivation rate constant and longer half-life. The enhancement of thermodynamic parameters indicated that the immobilized laccase had better thermal stability than free laccase. The residual activity of immobilized laccase remained at about 50.0% after 30 days, which was 4.0 times that of free laccase. Immobilized laccase demonstrated excellent removal of phenolic pollutants (2,4-dichlorophenol, bisphenol A, phenol, and 4-chlorophenol) and perfect reusability with 70% removal efficiency retention for 2,4-dichlorophenol after seven cycles. These results suggested that immobilized laccase possessed great reusability, improved thermal stability, and excellent storage stability. Organic–inorganic nanomaterials have a good application prospect for laccase immobilization, and the immobilized laccase of this work may provide a practical application for the removal of phenolic pollutants.

Graphical abstract

Keywords

polydopamine / pollutant removal / thermodynamic / phenolic pollutants / immobilized laccase

References

[1] Zhou W, Zhang W, Cai Y. Laccase immobilization for water purification: a comprehensive review. Chemical Engineering Journal, 2020, 403: 126272

[2] Arora P K, Bae H. Bacterial degradation of chlorophenols and their derivatives. Microbial Cell Factories, 2014, 13(1): 1–17

[3] Rostami A, Abdelrasoul A, Shokri Z, Shirvandi Z. Applications and mechanisms of free and immobilized laccase in detoxification of phenolic compounds—a review. Korean Journal of Chemical Engineering, 2022, 39(4): 821–832

[4] Fan J X, Luo J Q, Wan Y H. Aquatic micro-pollutants removal with a biocatalytic membrane prepared by metal chelating affinity membrane chromatography. Chemical Engineering Journal, 2017, 327: 1011–1020

[5] Liu Y Y, Zeng Z T, Zeng G M, Tang L, Pang Y, Li Z, Liu C, Lei X X, Wu M S, Ren P Y, Liu Z, Chen M, Xie G. Immobilization of laccase on magnetic bimodal mesoporous carbon and the application in the removal of phenolic compounds. Bioresource Technology, 2012, 115: 21–26

[6] Fan J X, Luo J Q, Wan Y H. Membrane chromatography for fast enzyme purification, immobilization and catalysis: a renewable biocatalytic membrane. Journal of Membrane Science, 2017, 538: 68–76

[7] Bilal M, Ashraf S S, Cui J D, Lou W Y, Franco M, Mulla S I, Iqbal H M N. Harnessing the biocatalytic attributes and applied perspectives of nanoengineered laccases—a review. International Journal of Biological Macromolecules, 2021, 166: 352–373

[8] Qiu X, Qin J, Xu M, Kang L F, Hu Y. Organic–inorganic nanocomposites fabricated via functional ionic liquid as the bridging agent for laccase immobilization and its application in 2,4-dichlorophenol removal. Colloids and Surfaces B: Biointerfaces, 2019, 179: 260–269

[9] Sheldon R A, van Pelt S. Enzyme immobilisation in biocatalysis: why, what and how. Chemical Society Reviews, 2013, 42(15): 6223–6235

[10] Dicosimo R, Mcauliffe J, Poulose A J, Bohlmann G. Industrial use of immobilized enzymes. Chemical Society Reviews, 2013, 42(15): 6437–6474

[11] Zhao J X, Ma M M, Yan X H, Zhang G H, Xia J H, Zeng Z L, Yu P, Deng Q, Gong D M. Green synthesis of polydopamine functionalized magnetic mesoporous biochar for lipase immobilization and its application in interesterification for novel structured lipids production. Food Chemistry, 2022, 379: 132148

[12] Zhong L, Feng Y X, Wang G Y, Wang Z Y, Bilal M, Lv H X, Jia S R, Cui J D. Production and use of immobilized lipases in/on nanomaterials: a review from the waste to biodiesel production. International Journal of Biological Macromolecules, 2020, 152: 207–222

[13] Jeelani P G, Mulay P, Venkat R, Ramalingam C. Multifaceted application of silica nanoparticles: a review. Silicon, 2020, 12(6): 1337–1354

[14] Silvestri B, Vitiello G, Luciani G, Calcagno V, Costantini A, Gallo M, Parisi S, Paladino S, Iacomino M, D’Errico G, Caso M F, Pezzella A, d’Ischia M. Probing the eumelanin-silica interface in chemically engineered bulk hybrid nanoparticles for targeted subcellular antioxidant protection. ACS Applied Materials & Interfaces, 2017, 9(43): 37615–37622

[15] Ni Y, Lv Z X, Wang Z, Kang S Y, He D W, Liu R J. Immobilization and evaluation of penicillin G acylase on hydroxy and aldehyde functionalized magnetic α-Fe₂O₃/Fe₃O₄ heterostructure nanosheets. Frontiers in Bioengineering and Biotechnology, 2022, 9(1): 812403

[16] Lin J, Liu Y, Shi C, Le X, Zhou X, Zhao Z, Ou Y, Yang J. Reversible immobilization of laccase onto metal-ion-chelated magnetic microspheres for bisphenol A removal. International Journal of Biological Macromolecules, 2016, 84: 189–199

[17] Chen Y, Ding H, Wang B, Shi Q, Gao J, Cui Z, Wan Y. Dopamine functionalization for improving crystallization behaviour of polyethylene glycol in shape-stable phase change material with silica fume as the matrix. Journal of Cleaner Production, 2019, 208: 951–959

[18] Wang L, Shi Y, Chen S, Wang W, Tian M, Ning N, Zhang L. Highly efficient mussel-like inspired modification of aramid fibers by UV-accelerated catechol/polyamine deposition followed chemical grafting for high-performance polymer composites. Chemical Engineering Journal, 2017, 314: 583–593

[19] Deng M, Zhao H, Zhang S, Tian C, Zhang D, Du P, Liu C, Cao H, Li H. High catalytic activity of immobilized laccase on core-shell magnetic nanoparticles by dopamine self-polymerization. Journal of Molecular Catalysis B: Enzymatic, 2015, 112: 15–24

[20] Chen H, Hao Z, Li Y, Li Y, Wang X. Facile synthesis of oxidic PEG-modified magnetic polydopamine nanospheres for candida rugosa lipase immobilization. Applied Microbiology and Biotechnology, 2015, 99(3): 1249–1259

[21] Chen Y, Jiang Y, Gao J, Wu W, Dong L, Yang Z. Facile immobilization of nitrile hydratase in SBA-15 via a biomimetic coating. Journal of Porous Materials, 2017, 24(3): 787–793

[22] Zhang H R, Luo J Q, Li S S, Wei Y P, Wan Y H. Biocatalytic membrane based on polydopamine coating: a platform for studying immobilization mechanisms. Langmuir, 2018, 34(8): 2585–2594

[23] Khan M K, Luo J Q, Wang Z S, Khan R, Chen X R, Wan Y H. Alginate dialdehyde meets nylon membrane: a versatile platform for facile and green fabrication of membrane adsorbers. Journal of Materials Chemistry B: Materials for Biology and Medicine, 2018, 6(11): 1640–1649

[24] Wang S S, Li S, Liu R T, Zhang W, Xu H J, Hu Y. Immobilization of interfacial activated candida rugosa lipase onto magnetic chitosan using dialdehyde cellulose as cross-linking agent. Frontiers in Bioengineering and Biotechnology, 2022, 10: 946117

[25] Ran F, Zou Y, Xu Y, Liu X, Zhang H. Fe₃O₄@MoS₂@PEI-facilitated enzyme tethering for efficient removal of persistent organic pollutants in water. Chemical Engineering Journal, 2019, 375(1): 121947

[26] Xia T T, Liu C Z, Hu J H, Guo C. Improved performance of immobilized laccase on amine-functioned magnetic Fe₃O₄ nanoparticles modified with polyethylenimine. Chemical Engineering Journal, 2016, 295: 201–206

[27] Yang X Y, Chen Y F, Yao S, Qian J Q, Guo H, Cai X H. Preparation of immobilized lipase on magnetic nanoparticles dialdehyde starch. Carbohydrate Polymers, 2019, 218: 324–332

[28] Qiu X, Wang Y, Xue Y, Li W X, Hu Y. Laccase immobilized on magnetic nanoparticles modified by amino-functionalized ionic liquid via dialdehyde starch for phenolic compounds biodegradation. Chemical Engineering Journal, 2020, 391: 123564

[29] Tang R, Du Y, Fan L. Dialdehyde starch-crosslinked chitosan films and their antimicrobial effects. Journal of Polymer Science Part B: Polymer Physics, 2003, 41(9): 993–997

[30] Gao J, Zhou J, Zhang X, Shi Q, Han Z, Chen Y. Facile functionalized mesoporous silica using biomimetic method as new matrix for preparation of shape: tabilized phase-change material with improved enthalpy. International Journal of Energy Research, 2019, 43(14): 8649–8659

[31] Bradford M M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Analytical Biochemistry, 1976, 72(1-2): 248–254

[32] Wahab W A A, Karam E A, Hassan M E, Kansoh A L, Esawy M A, Awad G E A. Optimization of pectinase immobilization on grafted alginate-agar gel beads by 2(4) full factorial CCD and thermodynamic profiling for evaluating of operational covalent immobilization. International Journal of Biological Macromolecules, 2018, 113: 159–170

[33] Birhanli E, Noma S A A, Boran F, Ulu A, Yesilada O, Ates B. Design of laccase–metal–organic framework hybrid constructs for biocatalytic removal of textile dyes. Chemosphere, 2022, 292: 133382

[34] Gascón V, Márquez-Álvarez C, Blanco R M. Efficient retention of laccase by non-covalent immobilization on amino-functionalized ordered mesoporous silica. Applied Catalysis A: General, 2014, 482: 116–126

[35] Xiang X R, Ding S, Suo H B, Xu C, Gao Z, Hu Y. Fabrication of chitosan-mesoporous silica SBA-15 nanocomposites via functional ionic liquid as the bridging agent for PPL immobilization. Carbohydrate Polymers, 2018, 182: 245–253

[36] Guo H, Lei B S, Yu J W, Chen Y F, Qian J Q. Immobilization of lipase by dialdehyde cellulose crosslinked magnetic nanoparticles. International Journal of Biological Macromolecules, 2021, 185: 287–296

[37] Chen C, Sun W, Lv H Y, Li H, Wang Y B, Wang P. Spacer arm-facilitated tethering of laccase on magnetic polydopamine nanoparticles for efficient biocatalytic water treatment. Chemical Engineering Journal, 2018, 350: 949–959

[38] Hu T G, Cheng J H, Zhang B B, Lou W Y, Zong M H. Immobilization of alkaline protease on amino-functionalized magnetic nanoparticles and its efficient use for preparation of oat polypeptides. Industrial & Engineering Chemistry Research, 2015, 54(17): 4689–4698

[39] Xie W L, Zang X Z. Lipase immobilized on ionic liquid-functionalized magnetic silica composites as a magnetic biocatalyst for production of trans-free plastic fats. Food Chemistry, 2018, 257: 15–22

[40] Hou C, Qi Z G, Zhu H. Preparation of core–shell magnetic polydopamine/alginate biocomposite for candida rugosa lipase immobilization. Colloids and Surfaces B: Biointerfaces, 2015, 128: 544–551

[41] Liu R J, Huang W, Pan S, Li Y, Yu L L, He D W. Covalent immobilization and characterization of penicillin G acylase on magnetic Fe₂O₃/Fe₃O₄ heterostructure nanoparticles prepared via a novel solution combustion and gel calcination process. International Journal of Biological Macromolecules, 2020, 162(21): 1587–1596

[42] Huang W, Pan S, Li Y, Yu L L, Liu R J. Immobilization and characterization of cellulase on hydroxy and aldehyde functionalized magnetic Fe₂O₃/Fe₃O₄ nanocomposites prepared via a novel rapid combustion process. International Journal of Biological Macromolecules, 2020, 162(21): 845–852

[43] Dhiman S, Srivastava B, Singh G, Khatri M, Arya S K. Immobilization of mannanase on sodium alginate-grafted-beta-cyclodextrin: an easy and cost effective approach for the improvement of enzyme properties. International Journal of Biological Macromolecules, 2020, 156: 1347–1358

[44] Ahmed S A, Saleh S A A, Abdel-Hameed S A M, Fayad A M. Catalytic, kinetic and thermodynamic properties of free and immobilized caseinase on mica glass-ceramics. Heliyon, 2019, 5(5): 1–12

[45] Wehaidy H R, Abdel-Naby M A, El-Hennawi H M, Youssef H F. Nanoporous zeolite-x as a new carrier for laccase immobilization and its application in dyes decolorization. Biocatalysis and Agricultural Biotechnology, 2019, 19: 101135

[46] Qiu X, Wang S S, Miao S S, Suo H B, Xu H J, Hu Y. Co-immobilization of laccase and ABTS onto amino-functionalized ionic liquid-modified magnetic chitosan nanoparticles for pollutants removal. Journal of Hazardous Materials, 2021, 401: 123353

[47] Wu E H, Li Y X, Huang Q, Yang Z K, Wei A Y, Hu Q. Laccase immobilization on amino-functionalized magnetic metal organic framework for phenolic compound removal. Chemosphere, 2019, 233: 327–335

[48] Chao C, Liu J D, Wang J T, Zhang Y W, Zhang B, Zhang Y T, Xiang X, Chen R F. Surface modification of halloysite nanotubes with dopamine for enzyme immobilization. ACS Applied Materials & Interfaces, 2013, 5(21): 10559–10564

[49] Mohammadi M, As’habi M A, Salehi P, Yousefi M, Nazari M, Brask J. Immobilization of laccase on epoxy-functionalized silica and its application in biodegradation of phenolic compounds. International Journal of Biological Macromolecules, 2018, 109: 443–447

[50] Pang R, Li M Z, Zhang C D. Degradation of phenolic compounds by laccase immobilized on carbon nanomaterials: diffusional limitation investigation. Talanta, 2015, 131: 38–45

[51] Ren D J, Jiang S, Fu L J, Wang Z B, Zhang S Q, Zhang X Q, Gong X Y, Chen W S. Laccase immobilized on amino-functionalized magnetic Fe₃O₄–SiO₂ core–shell material for 2,4-dichlorophenol removal. Environmental Technology, 2021, 3: 1–22

[52] Chen Z H, Yao J, Ma B, Liu B, Kim J, Li H, Zhu X Z, Zhao C C, Amde M. A robust biocatalyst based on laccase immobilized superparamagnetic Fe₃O₄@SiO₂-NH₂ nanoparticles and its application for degradation of chlorophenols. Chemosphere, 2022, 291(1): 132727

[53] Huan W W, Yang Y X, Wu B, Yuan H M, Zhang Y N, Liu X N. Degradation of 2,4-DCP by theimmobilized laccase on the carrier of Fe₃O₄@SiO₂-NH₂. Chinese Journal of Chemistry, 2012, 30(12): 2849–2860

[54] Yang J, Hu Y, Jiang L, Zou B, Jia R, Huang H. Enhancing the catalytic properties of porcine pancreatic lipase by immobilization on SBA-15 modified by functionalized ionic liquid. Biochemical Engineering Journal, 2013, 70: 46–54

RIGHTS & PERMISSIONS

Higher Education Press