DOI QR코드

DOI QR Code

Laccase Immobilization on Copper-Magnetic Nanoparticles for Efficient Bisphenol Degradation

  • Sanjay K. S. Patel (Department of Chemical Engineering, Konkuk University) ;
  • Vipin C. Kalia (Department of Chemical Engineering, Konkuk University) ;
  • Jung-Kul Lee (Department of Chemical Engineering, Konkuk University)
  • Received : 2022.10.19
  • Accepted : 2022.11.05
  • Published : 2023.01.28

Abstract

Laccase activity is influenced by copper (Cu) as an inducer. In this study, laccase was immobilized on Cu and Cu-magnetic (Cu/Fe2O4) nanoparticles (NPs) to improve enzyme stability and potential applications. The Cu/Fe2O4 NPs functionally activated by 3-aminopropyltriethoxysilane and glutaraldehyde exhibited an immobilization yield and relative activity (RA) of 93.1 and 140%, respectively. Under optimized conditions, Cu/Fe2O4 NPs showed high loading of laccase up to 285 mg/g of support and maximum RA of 140% at a pH 5.0 after 24 h of incubation (4℃). Immobilized laccase, as Cu/Fe2O4-laccase, had a higher optimum pH (4.0) and temperature (45℃) than those of a free enzyme. The pH and temperature profiles were significantly improved through immobilization. Cu/Fe2O4-laccase exhibited 25-fold higher thermal stability at 65℃ and retained residual activity of 91.8% after 10 cycles of reuse. The degradation of bisphenols was 3.9-fold higher with Cu/Fe2O4-laccase than that with the free enzyme. To the best of our knowledge, Rhus vernicifera laccase immobilization on Cu or Cu/Fe2O4 NPs has not yet been reported. This investigation revealed that laccase immobilization on Cu/Fe2O4 NPs is desirable for efficient enzyme loading and high relative activity, with remarkable bisphenol A degradation potential.

Keywords

Acknowledgement

This study was supported by the Basic Science Research Program through the National Research Foundation of Korea (NRF) funded by the Ministry of Science, ICT & Future Planning (2019R1C1C11009766, 2021R1I1A1A01060963, and 2021H1D3A2A01099705). This work was also supported by the KU Research Professor Program of Konkuk University.

References

  1. Adamian Y, Lonappan L, Alokpa K, Agathos SN, Cabana H. 2021. Recent developments in the immobilization of laccase on carbonaceous supports for environmental applications - A critical review. Front. Bioeng. Biotechnol. 9: 778239.
  2. Zhu CY, Li FL, Zhang YW, Gupta RK, Patel SKS, Lee JK. 2022. Recent strategies for immobilization of therapeutic enzymes. Polymers 14: 1409.
  3. Gao H, Li J, Sivakumar D, Kim T-S, Patel SKS, Kalia VC, et al. 2019. NADH oxidase from Lactobacillus reuteri: A versatile enzyme for oxidized cofactor regeneration. Int. J. Biol. Macromol. 123: 629-636. https://doi.org/10.1016/j.ijbiomac.2018.11.096
  4. Patel SKS, Choi H, Lee J-K. 2019. Multimetal-based inorganic-protein hybrid system for enzyme immobilization. ACS Sustainable Chem. Eng. 7: 13633-13638. https://doi.org/10.1021/acssuschemeng.9b02583
  5. Kumar A, Patel SKS, Mardan B, Pagolu R, Lestari R, Jeong S-H, et al. 2018. Immobilization of xylanase using a protein-inorganic hybrid system. J. Microbiol. Biotechnol. 28: 638-644. https://doi.org/10.4014/jmb.1710.10037
  6. Durate D, Casadio R, Martelli L, Tasco G, Portaccio M, Luca PD, et al. 2004. Isothermal and non-isothermal bioreactors in the detoxification of waste waters polluted by aromatic compounds by means of immobilised laccase from Rhus vernicifera. J. Mol. Catal. B Enzym. 27: 191-206. https://doi.org/10.1016/j.molcatb.2003.11.008
  7. Patel SKS, Choi SH, Kang YC, Lee JK. 2017. Eco-friendly composite of Fe3O4-reduced graphene oxide particles for efficient enzyme immobilization. ACS Appl. Mater. Inter. 9: 2213-2222. https://doi.org/10.1021/acsami.6b05165
  8. Kumar A, Park GD, Patel SKS, Kondaveeti S, Otari S, Anwar MZ, et al. 2019. SiO2 microparticles with carbon nanotube-derived mesopores as an efficient support for enzyme immobilization. Chem. Eng. J. 359: 1252-1264. https://doi.org/10.1016/j.cej.2018.11.052
  9. Yang WY, Min DY, Wen SX, Jin L, Rong L, Tetsuo M, et al. 2006. Immobilization and characterization of laccase from Chinese Rhus vernicifera on modified chitosan. Process Biochem. 41: 1378-1382. https://doi.org/10.1016/j.procbio.2006.01.018
  10. Chen Z, Oh WD, Yap PS. 2022. Recent advances in the utilization of immobilized laccase for the degradation of phenolic compounds in aqueous solutions: A review. Chemosphere 307: 135824.
  11. Lee HR, Chung M, Kim MI, Ha SH. 2017. Preparation of glutaraldehyde-treated lipase-inorganic hybrid nanoflowers and their catalytic performance as immobilized enzymes. Enzyme Microb. Technol. 105: 24-29. https://doi.org/10.1016/j.enzmictec.2017.06.006
  12. Patel SKS, Anwar MZ, Kumar A, Otari SV, Pagolu RT, Kim SY, et al. 2018. Fe2O3 yolk-shel particle-based laccase biosensor for efficient detection of 2,6-dimethoxyphenol. Biochem. Eng. J. 132: 1-8. https://doi.org/10.1016/j.bej.2017.12.013
  13. Suman SK, Patnam PL, Ghosh S, Jain SL. 2019. Chicken feather derived novel support material for immobilization of laccase and its application in oxidation of veratryl alcohol. ACS Sustain. Chem. Eng. 7: 3464-3474. https://doi.org/10.1021/acssuschemeng.8b05679
  14. Patel SKS, Kalia VC, Kim SY, Lee JK, Kim IW. 2022. Immobilization of laccase through inorganic-protein hybrids using various metal ions. Indian J. Microbiol. 62: 312-316. https://doi.org/10.1007/s12088-022-01000-5
  15. Kumar V, Patel SKS, Gupta RK, Otari SV, Gao H, Lee JK, et al. 2019. Enhanced saccharification and fermentation of rice straw by reducing the concentration of phenolic compounds using an immobilized enzyme cocktail. Biotechnol. J. 14: 1800468.
  16. Latif A, Maqbool A, Sun K, Si Y. 2022. Immobilization of Trametes versicolor laccase on Cu-alginate beads for biocatalytic degradation of bisphenol A in water: Optimized immobilization, degradation and toxicity assessment. J. Environ. Chem. Eng. 10: 107089.
  17. Fernandez-Fernandez M, Sanroman MA, Moldes D. 2013. Recent developments and applications of immobilized laccase. Biotechnol. Adv. 31: 1808-1825. https://doi.org/10.1016/j.biotechadv.2012.02.013
  18. Zhou W, Zhang W, Cai Y. 2021. Laccase immobilization for water purification: a comprehensive review. Chem. Eng. J. 403: 126272.
  19. Li C, Nguyen LN, Hou J, Hai FI, Chen V. 2017. Direct immobilization of laccase on titania nanoparticles from crude enzyme extracts of P. ostreatus culture for micro-pollutant degradation. Sep. Purif. Technol. 178: 215-223. https://doi.org/10.1016/j.seppur.2017.01.043
  20. Daronch NA, Kelbert M, Pereira CS, de Araujo PHH, de Oliveira D. 2020. Elucidating the choice for a precise matrix for laccase immobilization: a review. Chem. Eng. J. 397: 125506.
  21. Otari SV, Patel SKS, Kim SY, Haw JR, Kalia VC, Kim IW, et al. 2019. Copper ferrite magnetic nanoparticles for the immobilization of enzyme. Indian J. Microbiol. 59: 105-108. https://doi.org/10.1007/s12088-018-0768-3
  22. Pandey D, Daverey A, Dutta K, Arunachalam K. 2022. Bioremoval of toxic malachite green from water through simultaneous decolorization and degradation using laccase immobilized biochar. Chemosphere 297: 134126.
  23. Patel SKS, Otari SV, Li J, Kim DR, Kim SC, Cho BK, et al. 2018. Synthesis of cross-linked protein-metal hybrid nanoflowers and its application in repeated batch decolorization of synthetic dyes. J. Hazard. Mater. 347: 442-450. https://doi.org/10.1016/j.jhazmat.2018.01.003
  24. Liang S, Wu XL, Xiong J, Yuan X, Liu SL, Zong MH, et al. 2022. Multivalent Ce-MOFs as biomimetic laccase nanozyme for environmental remediation. Chem. Eng. J. 450: 138220.
  25. Molina MA, Diez-Jaen J, Sanchez-Sanchez M, Blano, RM. 2022. One-pot laccase@MOF biocatalysts efficiently remove bisphenol A from water. Catal. Today 390-391: 265-271. https://doi.org/10.1016/j.cattod.2021.10.005
  26. Wang Z, Ren D, Cheng Y, Zhang X, Zhang S, Chen W. 2022. Immobilization of laccase on chitosan functionalized halloysite nanotubes for degradation of bisphenol A in aqueous solution: degradation mechanism and mineralization pathway. Heliyon 8: e09919.
  27. Ran F, Zou Y, Xu Y, Liu X, Zhang H. 2019. Fe3O4@MoS2@PEI-facilitated enzyme tethering for efficient removal of persistent organic pollutants in water. Chem. Eng. J. 375: 121947.
  28. Tarasi R, Alipour M, Gorgannezhad L, Imanparast S, Yousefi-Ahmadipour A, Ramezani A, et al. 2018. Laccase immobilization onto magnetic β-cyclodextrin-modified chitosan: improved enzyme stability and efficient performance for phenolic compounds elimination. Macromol. Res. 26: 755-762. https://doi.org/10.1007/s13233-018-6095-z
  29. Zhang C, You S, Liu Y, Wang C, Yan Q, Qi W, et al. 2020. Construction of luffa sponge-based magnetic carbon nanocarriers for laccase immobilization and its application in the removal of bisphenol A. Bioresour. Technol. 305: 123085.
  30. Patel SKS, Kalia VC, Choi JH, Haw JR, Kim IW, Lee JK. 2014. Immobilization of laccase on SiO2 nanocarriers improves its stability and reusability. J. Microbiol. Biotechnol. 24: 639-647. https://doi.org/10.4014/jmb.1401.01025
  31. Olshansky Y, Masaphy S, Root RA, Rytwo G. 2018. Immobilization of Rhus vernicifera laccase on sepiolite; effect of chitosan and copper modification on laccase adsorption and activity. Appl. Clay Sci. 152: 143-147. https://doi.org/10.1016/j.clay.2017.11.006
  32. Suman SK, Malhotra M, Khichi SS, Ghosh S, Jain SL. 2020. Optimization and kinetic modeling of Trametes maxima IIPLC-32 laccase and application in recalcitrant dye decolorization. New J. Chem. 45: 2110-2121. https://doi.org/10.1039/D0NJ05179A
  33. Tran TD, Nguyen PT, Le TN, Kim MI. 2021. DNA-copper hybrid nanoflowers as efficient laccase mimics for colorimetric detection of phenolic compounds in paper microfluidic devices. Biosens. Bioelectron. 182: 113187.
  34. Le TN, Le XA, Tran TD, Lee KJ, Kim MI. 2022. Laccase-mimicking Mn-Cu hybrid nanoflowers for paper-based visual detection of phenolic neurotransmitters and rapid degradation of dyes. J. Nanotchnol. 20: 358.
  35. Patel SKS, Choi SH, Kang YC, Lee JK. 2016. Large-scale aerosol-assisted synthesis of biofriendly Fe2O3 yolk-shell particles: a promising support for enzyme immobilization. Nanoscale 8: 6728-6738. https://doi.org/10.1039/C6NR00346J
  36. Patel SKS, Gupta RK, Kim SY, Kim IW, Kalia VC, Lee JK. 2021. Rhus vernicifera laccase immobilization on magnetic nanoparticles to improve stability and its potential application in bisphenol A degradation. Indian J. Microbiol. 61: 45-54. https://doi.org/10.1007/s12088-020-00912-4
  37. Wan, YY, Lu R, Akiyama K, Okamoto K, Honda T, Du YM, et al. 2010. Effects of lacquer polysaccharides, glycoproteins and isoenzymes on the activity of free and immobilised laccase from Rhus vernicifera. Int. J. Biol. Macromol. 47: 76-81. https://doi.org/10.1016/j.ijbiomac.2010.03.016
  38. Kondaveeti S, Pagolu R, Patel SKS, Kumar A, Bisht A, Dad D, et al. 2019. Bioelectrochemical detoxification of phenolic compounds during enzymatic pre-treatment of rice straw. J. Microbiol. Biotechnol. 29: 1760-1768. https://doi.org/10.4014/jmb.1909.09042
  39. Rouhani S, Rostami A, Salimi A, Pourshiani O. 2018. Graphene oxide/CuFe2 nanocomposite as a novel scaffold for the immobilization of laccase and its application as a recyclable nanobiocatalyst for the green synthesis of arylsulfonyl benzenediols. Biochem. Eng. J. 133: 1-11. https://doi.org/10.1016/j.bej.2018.01.004
  40. Lu R, Miyakoshi T. 2012. Studies on acetone powder and purified Rhus laccase immobilized on zirconium chloride for oxidation of phenols. Enzyme Res. 2012: 375309.
  41. Georgieva S, Godjevargova T, Portaccio M, Lepore M, Mita DG. 2008. Advantages in using non-isothermal bioreactors in bioremediation of water polluted by phenol by means of immobilized laccase from Rhus vernicifera. J. Mol. Catal. B Enzym. 55: 177-184. https://doi.org/10.1016/j.molcatb.2008.03.011
  42. Kumar A, Kim IW, Patel SKS, Lee JK. 2018. Synthesis of protein-inorganic nanohybrids with improved catalytic properties using Co3(PO4)2. Indian J. Microbiol. 58: 100-104.  https://doi.org/10.1007/s12088-017-0700-2