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Immobilization of laccase on carboxyl-functionalized chitosan-coated magnetic nanoparticles with improved stability and reusability

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Abstract

Enzyme immobilization can improve the catalytic activity and stability against temperature, pH, and various environmental conditions. In this study, carboxyl-functionalized chitosan-coated magnetic nanoparticle was synthesized and used as a support for the immobilization of laccase. The synthesized nanoparticle was characterized by transmission electron microscopy and FT-IR spectroscopy. In order to investigate the stability of the enzyme to pH changes, the activities of free and immobilized enzymes were measured at different pH values ranging from 2.0 to 8.0. The thermal stability and storage stability of the enzymes were also studied. Kinetic parameters and reusability were evaluated for both free and immobilized enzymes. The results showed that the magnetic nanoparticles and carboxyl-functionalized chitosan-coated magnetic nanoparticles are spherical with dispersed size distribution and zeta-potential of − 33.4 and + 1.95 mV, respectively. Based on our observations, the maximum activity of the enzyme was shifted toward higher temperatures after the immobilization. Furthermore, the immobilized laccase retained 80% of its initial activity after 120 days, while free enzyme maintained only 50% of its initial activity during the same period. The values of Michealis-Menten constant and maximum velocity for immobilized laccase were 0.113 mM and 1.27 µM min−1, respectively, whereas the values for free enzyme were 0.093 mM and 1.79 µM min−1, respectively. Both free and immobilized laccase exhibited optimum activities at pH 3.0 and decreasing trends were found at pH values more than 5 but immobilized laccase preserved its high activity at a wide range of pH compared with that of free laccase. In particular, it can be used at higher temperatures and broader pH with improved storage stability and reusability, demonstrating the superior potential of bioremediation utilizing this immobilization method.

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Data availability statement

All data generated or analysed during this study are included in this published article.

References

  1. Silva C, Martins M, Jing S, Fu J, Cavaco-Paulo A (2018) Crit Rev Biotechnol 38:335

    CAS  PubMed  Google Scholar 

  2. Tarasi R, Alipour M, Gorgannezhad L, Imanparast S, Yousefi-Ahmadipour A, Ramezani A, Ganjali MR, Shafiee A, Faramarzi MA, Khoobi M (2018) Macromol Res 26:755

    CAS  Google Scholar 

  3. Zhang K, Yang W, Liu Y, Zhang K, Chen Y, Yin X (2020) J Mol Struct 1220:128769

    CAS  Google Scholar 

  4. Chen X, He B, Feng M, Zhao D, Sun J (2020) Chin J Chem Eng 28:2152

    CAS  Google Scholar 

  5. Nguyen HH, Kim M (2017) Appl Sci Converg Technol 26:157

    Google Scholar 

  6. Jamil F, Asgher M, Hussain F, Bhatti HN (2018) J Animal Plant Sci 28:2

    Google Scholar 

  7. Qiu X, Wang S, Miao S, Suo H, Xu H, Hu Y (2021) J Hazard Mater 401:123353

    CAS  PubMed  Google Scholar 

  8. Dal Magro L, Pessoa JPS, Klein MP, Fernandez-Lafuente R, Rodrigues RC (2021) Catal Today 362:184

    Google Scholar 

  9. Ashjari M, Garmroodi M, Asl FA, Emampour M, Yousefi M, Lish MP, Habibi Z, Mohammadi M (2020) Process Biochem 90:156

    CAS  Google Scholar 

  10. Fernandez-Lafuente R (2009) Technol 45:405

    CAS  Google Scholar 

  11. Sannino F, Costantini A, Ruffo F, Aronne A, Venezia V, Califano V (2020) J Nanomater 10:108

    CAS  Google Scholar 

  12. Janusz G, Pawlik A, Świderska-Burek U, Polak J, Sulej J, Jarosz-Wilkołazka A, Paszczyński A (2013) Int J Mol Sci 21:966

    Google Scholar 

  13. Costa JB, Lima MJ, Sampaio MJ, Neves MC, Faria JL, Morales-Torres S, Tavares AP, Silva CG (2019) J Chem Eng 355:974

    CAS  Google Scholar 

  14. Kim HJ, Jin JN, Kan E, Kim KJ, Lee SH (2017) Biotechnol Bioproc E 22:89

    CAS  Google Scholar 

  15. Mogharabi M, Nassiri-Koopaei N, Bozorgi-Koushalshahi M, Nafissi-Varcheh N, Bagherzadeh G, Faramarzi. (2012) Immobilization of laccase in alginate-gelatin mixed gel and decolorization of synthetic dyes. Bioinorg Chem Appl 2012:823830

    PubMed Central  PubMed  Google Scholar 

  16. Xing X, Han Y, Jiang Q, Sun Y, Wang X, Qu G, Sun G, Li Y (2021) Cellulose 28:4793

    CAS  Google Scholar 

  17. Liu DM, Dong C (2020) Process Biochem 92:464

    Google Scholar 

  18. Vaghari H, Jafarizadeh-Malmiri H, Mohammadlou M, Berenjian A, Anarjan N, Jafari N, Nasiri S (2015) Biotechnol Lett 38:223

    PubMed  Google Scholar 

  19. Xia TT, Liu CZ, Hu JH, Guo C (2016) J Chem Eng 295:201

    CAS  Google Scholar 

  20. Sun J, Yang L, Jiang M, Xu B (2017) J Chromatogr B 1054:57

    CAS  Google Scholar 

  21. Wu M, Long Z, Xiao H, Dong C (2016) Carbohydr Res 434:27

    CAS  PubMed  Google Scholar 

  22. Chang YC, Chen DH (2005) Macromol Biosci 5:254

    CAS  PubMed  Google Scholar 

  23. Nouri M (2020) Biocatal Agric Biotechnol 29:101681

    Google Scholar 

  24. Bertrand T, Jolivalt C, Briozzo P, Caminade E, Joly N, Madzak C, Mougin C (2002) Biochem J 41:7325

    CAS  Google Scholar 

  25. Parandhaman T, Pentela N, Ramalingam B, Samanta D, Das SK (2017) ACS Sustain Chem Eng 5:489

    CAS  Google Scholar 

  26. Aydemir T, Güler S (2015) Artif Cells Nanomed Biotechnol 43:425

    CAS  PubMed  Google Scholar 

  27. Jiang DS, Long SY, Huang J, Xiao HY, Zhou JY (2005) Biochem Eng J 25:15

    Google Scholar 

  28. Abdollahi M, Zeinali S, Nasirimoghaddam S, Sabbaghi S (2015) Desalin Water Treat 56:2092

    CAS  Google Scholar 

  29. Das A, Singh J, Yogalakshmi KN (2019) Int Biodeterior Biodegrad 117:183

    Google Scholar 

  30. Zhu A, Yuan L, Liao T (2007) Int J Pharm 350:361

    PubMed  Google Scholar 

  31. Ding Y, Shen SZ, Sun H, Sun K, Liu F, Qi Y, Yan J (2015) Mater Sci Eng C 48:487

    CAS  Google Scholar 

  32. López-Cruz A, Barrera C, Calero-DdelC VL, Rinaldi C (2009) J Mater Chem 19:6870

    Google Scholar 

  33. Mohammadi M, Ashabi MA, Salehi P, Yousefi M, Nazari M, Brask J (2018) J Biol Macromol 109:443

    CAS  Google Scholar 

  34. Sampaio LM, Padrão J, Faria J, Silva JP, Silva CJ, Dourado F, Zille A (2016) Carbohydr Polym 145:1

    CAS  PubMed  Google Scholar 

  35. Jaiswal N, Pandey VP, Dwivedi UN (2016) Int J Biol Macromol 86:288

    CAS  PubMed  Google Scholar 

  36. Fernandes RA, Daniel-da-Silva AL, Tavares AP, Xavier AM (2017) Chem Eng Sci 158:599

    CAS  Google Scholar 

  37. Nicolucci C, Rossi S, Menale C, Godjevargova T, Ivanov Y, Bianco M, Mita L, Bencivenga U, Mita DG, Diano N (2011) Biodegradation 22:673

    CAS  PubMed  Google Scholar 

  38. Aricov L, Leonties AR, Gîfu IC, Preda D, Raducan A, Anghel DF (2020) J Environ Manage 276:111326

    CAS  PubMed  Google Scholar 

  39. Rekuć A, Jastrzembska B, Liesiene J, Bryjak J (2009) J Mol Catal B Enzym 57:216

    Google Scholar 

  40. Fortes CC, Daniel-da-Silva AL, Xavier AM, Tavares AP (2017) Chem Eng Process 117:1

    CAS  Google Scholar 

  41. Alver E, Metin AÜ (2017) Int Biodeterior Biodegradation 125:235

    CAS  Google Scholar 

  42. Bilal M, Asgher M (2016) J Mol Catal B Enzym 128:82

    CAS  Google Scholar 

  43. Bilal M, Asgher M, Shahid M, Bhatti HN (2016) Int J Biol Macromol 86:728

    CAS  PubMed  Google Scholar 

  44. Mohidem NA, Bin Mat H (2012) J Sol-Gel Sci Technol 61:96

    CAS  Google Scholar 

  45. Ulu A, Birhanli E, Boran F, Köytepe S, Yesilada O, Ateş B (2020) Int J Biol Macromol 150:871

    CAS  PubMed  Google Scholar 

  46. Silveira TR, Ebling CD, Dal Magro L, Rodrigues RC, Schneider WDH, Camassola M, de Menezes EW, Meneguzzi Á, Klein MP (2020) Biocatal Agric Biotechnol 30:101859

    Google Scholar 

  47. Fang H, Huang J, Ding L, Li M, Chen Z (2009) J Wuhan Univ Technol Mater Sci Ed 24:42

    CAS  Google Scholar 

  48. Xu R, Zhou Q, Li F, Zhang B (2013) J Chem Eng 222:321

    CAS  Google Scholar 

  49. Kunamneni A, Ghazi I, Camarero S, Ballesteros A, Plou FJ, Alcalde M (2008) Process Biochem 43:169

    CAS  Google Scholar 

  50. Asgher M, Noreen S, Bilal M (2017) Chem Eng Res Des 119:1

    CAS  Google Scholar 

  51. Huang J, Liu C, Xiao H, Wang J, Jiang D, Gu E (2007) Int J Nanomedicine 2:775

    CAS  PubMed Central  PubMed  Google Scholar 

  52. Wang Y, Zhang D, He FR, Chen XC (2011) Chin Chem Lett 23:197

    Google Scholar 

  53. Zhu Y, Kaskel S, Shi J, Wage T, van Pée KH (2007) Chem Mater 19:6408

    CAS  Google Scholar 

  54. Bayramoğlu G, Arıca MY (2009) Mater Sci Eng C 29:1990

    Google Scholar 

  55. Caramori SS, Fernandes KF (2008) Mater Sci Eng C 28:1159

    CAS  Google Scholar 

  56. Metin AÜ (2013) Macromol Res 21:1145

    CAS  Google Scholar 

  57. Muthuvelu KS, Rajarathinam R, Selvaraj RN, Rajendren VB (2020) Int J Biol Macromol 152:1098

    Google Scholar 

  58. Perwez M, Ahmad R, Sardar M (2017) Int J Biol Macromol 103:16

    CAS  PubMed  Google Scholar 

  59. Skoronski E, Fernandes M, Magalhães MDLB, Da Silva GF, João JJ, Soares CHL, Júnior AF (2014) Molecules 10:16794

    Google Scholar 

  60. Apriceno A, Silvestro I, Girelli A, Francolini I, Pietrelli L, Piozzi A (2021) Polymers 13:1453

    CAS  PubMed Central  PubMed  Google Scholar 

  61. Alsaiari NS, Amari A, Katubi KM, Alzahrani FM, Harharah HN, Rebah FB, Tahoon MA (2021) Appl Sci 11:8216

    CAS  Google Scholar 

  62. Zhou YT, Nie HL, Branford-White C, He ZY, Zhu LM (2009) J Colloid Interface Sci 330:29

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was carried out by the Biochemistry research laboratory of the university of Mazandaran. We would like to appreciate all the participants who took part in this investigation.

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Authors and Affiliations

  1. Department of Molecular and Cell Biology, Faculty of Basic Sciences, University of Mazandaran, Babolsar, Postal Code: 47416-95447, Iran

    Houman Maftoon & Ali Taravati

  2. Department of Medical Biotechnology, Faculty of Medicine, Babol University of Medical Sciences, Babol, Iran

    Fatemeh Tohidi

  3. Cellular and Molecular Biology Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran

    Fatemeh Tohidi

  4. Cancer Research Center, Health Research Institute, Babol University of Medical Sciences, Babol, Iran

    Fatemeh Tohidi

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  1. Houman Maftoon
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  2. Ali Taravati
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Correspondence to Ali Taravati.

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Maftoon, H., Taravati, A. & Tohidi, F. Immobilization of laccase on carboxyl-functionalized chitosan-coated magnetic nanoparticles with improved stability and reusability. Monatsh Chem 154, 279–291 (2023). https://doi.org/10.1007/s00706-022-03029-0

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