Abstract
An efficient heterogeneous natural polymer-based biocatalyst was fabricated through the immobilization of laccase onto dialdehyde inulin (DAI)-coated silica-caped magnetic nanoparticles (laccase@DAI@SiO2@Fe3O4⋅MNPs). The carrier was developed using SiO2@Fe3O4⋅MNPs and functionalized with DAI. The construction of immobilized laccase was confirmed by scanning electron microscopy (SEM) and Fourier transform infrared (FTIR) spectroscopy. Immobilization yield and efficiency were calculated as 61.0 ± 0.3% and 93.0 ± 0.6%, respectively. The immobilized laccase maintained 50% and 85% of its relative activity after 25 repeated cycles and 20 days of storage at 4 °C, respectively. The prepared biocatalyst effectively eliminated ofloxacin, a fluoroquinolone-type antibiotic, with a 63% removal capacity. Besides, antimicrobial activity study on some soil microorganisms involved in the biodegradation of xenobiotics revealed that the laccase-treated ofloxacin resulted in less toxic metabolites. The obtained data indicated that the fabricated biocatalyst is promising for the removal of ofloxacin or other analogs of fluoroquinolones in the environment.
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References
Ahmad R, Mirza A (2017) Inulin-folic acid/bentonite: a novel nanocomposite for confiscation of Cu (II) from synthetic and industrial wastewater. J Mol Liq 241:489–499. https://doi.org/10.1016/J.MOLLIQ.2017.05.125
Amin R, Khorshidi A, Shojaei AF, Rezaei S, Faramarzi MA (2018) Immobilization of laccase on modified Fe3O4@ SiO2@ Kit-6 magnetite nanoparticles for enhanced delignification of olive pomace bio-waste. Int J Biol Macromol 114:106–113. https://doi.org/10.1016/J.IJBIOMAC.2018.03.086
Asgher M, Noreen S, Bilal M (2017) Enhancing catalytic functionality of Trametes versicolor IBL-04 laccase by immobilization on chitosan microspheres. Chem Eng Res Des 119:1–11. https://doi.org/10.1016/j.cherd.2016.12.011
Ashrafi SD, Nasseri S, Alimohammadi M, Mahvi AH, Faramarzi MA (2020) Application of free and immobilized laccase for removal and detoxification of fluoroquinolones from aqueous solution. Glob NEST J 22:240–249
Ba S, Haroune L, Soumano L, Bellenger JP, Jones JP, Cabana H (2018) A hybrid bioreactor based on insolubilized tyrosinase and laccase catalysis and microfiltration membrane remove pharmaceuticals from wastewater. Chemosphere 201:749–755. https://doi.org/10.1016/j.chemosphere.2018.03.022
Baltierra-Trejo E, Márquez-Benavides L, Sánchez-Yáñez JM (2015) Inconsistencies and ambiguities in calculating enzyme activity: the case of laccase. J Microbiol Methods 119:126–131. https://doi.org/10.1016/j.mimet.2015.10.007
Bezerra CS, de Farias Lemos CMG, de Sousa M, Gonçalves LRB (2015) Enzyme immobilization onto renewable polymeric matrixes: past, present, and future trends. J Appl Polym Sci 132:42125. https://doi.org/10.1002/APP.42125
Daronch NA, Kelbert M, Pereira CS, de Araújo PHH, de Oliveira D (2020) Elucidating the choice for a precise matrix for laccase immobilization: a review. Chem Eng J 397:125506. https://doi.org/10.1016/j.cej.2020.125506
Datta S, Christena LR, Rajaram YRS (2013) Enzyme immobilization: an overview on techniques and support materials. 3Biotech 3:1–9. https://doi.org/10.1007/s13205-012-0071-7
Ding H, Wu Y, Zou B, Lou Q, Zhang W, Zhong J, Lu L, Dai G (2016) Simultaneous removal and degradation characteristics of sulfonamide, tetracycline, and quinolone antibiotics by laccase-mediated oxidation coupled with soil adsorption. J Hazard Mater 307:350–358. https://doi.org/10.1016/J.JHAZMAT.2015.12.062
García N, Benito E, Guzmán J, Tiemblo P, Morales V, García RA (2007) Functionalization of SBA-15 by an acid-catalyzed approach: a surface characterization study. Microporous Mesoporous Mater 106:129–139. https://doi.org/10.1016/j.micromeso.2007.02.043
Ge L, Li X, Zhang R, Yang T, Ye X, Li D, Mu C (2015) Development and characterization of dialdehyde xanthan gum crosslinked gelatin based edible films incorporated with amino-functionalized montmorillonite. Food Hydrocolloids 51:129–135. https://doi.org/10.1016/j.foodhyd.2015.04.029
Gładysz-Płaska A, Lipke A, Sternik D, Trytek M, Majdan M (2018) Spectroscopic, thermal and equilibrium characterization of U (VI) ions sorption on inulin in the presence of phosphates. J Mol Struct 1166:169–182. https://doi.org/10.1016/J.MOLSTRUC.2018.04.007
Guo H, Lei B, Yu J, Chen Y, Qian J (2021) Immobilization of lipase by dialdehyde cellulose crosslinked magnetic nanoparticles. Int J Biol Macromol 185:287–296. https://doi.org/10.1016/J.IJBIOMAC.2021.06.073
Gupta N, Jangid AK, Pooja D, Kulhari H (2019) Inulin: a novel and stretchy polysaccharide tool for biomedical and nutritional applications. Int J Biol Macromol 132:852–863. https://doi.org/10.1016/j.ijbiomac.2019.03.188
Hariri P, Jafari-Nodoushan H, Mojtabavi S, Hadizadeh N, Rezayaraghi F, Faramarzi MA (2022) Magnetic casein aggregates as an innovative support platform for laccase immobilization and bioremoval of crystal violet. Int J Biol Macromol 202:150–160. https://doi.org/10.1016/j.ijbiomac.2021.12.099
Kalaivani GJ, Suja SK (2016) TiO2 (rutile) embedded inulin—a versatile bio-nanocomposite for photocatalytic degradation of methylene blue. Carbohydr Polym 143:51–60. https://doi.org/10.1016/J.CARBPOL.2016.01.054
Kiani M, Mojtabavi S, Jafari-Nodoushan H, Tabib SR, Hassannejad N, Faramarzi MA (2022) Fast anisotropic growth of the biomineralized zinc phosphate nanocrystals for a facile and instant construction of laccase@Zn3(PO4)2 hybrid nanoflowers. Int J Biol Macromol. https://doi.org/10.1016/j.ijbiomac.2022.02.023
Ma W, Cao BK, Xu SN, Chen DM, Chen Y (2017) Activated carbon/polyvinyl formal sponge as a carrier for laccase immobilization for dyes decolourization. Mater Sci Eng. https://doi.org/10.1142/9789813226517_0049
Najafabadipour N, Mojtabavi S, Jafari-Nodoushan H, Samadi N, Faramarzi MA (2021) High efficiency of osmotically stable laccase for biotransformation and micro-detoxification of levofloxacin in the urea-containing solution: catalytic performance and mechanism. Colloids Surf B 207:112022. https://doi.org/10.1016/j.colsurfb.2021.112022
Noma SAA, Ulu A, Koytepe S, Ateş B (2020) Preparation and characterization of amino and carboxyl functionalized core-shell Fe3O4/SiO2 for L-asparaginase immobilization: a comparison study. Biocatal Biotransform 38:392–404. https://doi.org/10.1080/10242422.2020.1767605
Palanisamy S, Ramaraj SK, Chen SM, Yang TC, Yi-Fan P, Chen TW, Velusamy V, Selvam S (2017) A novel laccase biosensor based on laccase immobilized graphene-cellulose microfiber composite modified screen-printed carbon electrode for sensitive determination of catechol. Sci Rep 7:1–12. https://doi.org/10.1038/srep41214
Primožič M, Kravanja G, Knez Ž, Crnjac A, Leitgeb M (2020) Immobilized laccase in the form of (magnetic) cross-linked enzyme aggregates for sustainable diclofenac (bio) degradation. J Clean Prod 275:124121. https://doi.org/10.1016/J.JCLEPRO.2020.124121
Qi Y, Yang M, Xu W, He S, Men Y (2017) Natural polysaccharides-modified graphene oxide for adsorption of organic dyes from aqueous solutions. J Colloid Interface Sci 486:84–96. https://doi.org/10.1016/J.JCIS.2016.09.058
Qiu X, Wang Y, Xue Y, Li W, Hu Y (2020) Laccase immobilized on magnetic nanoparticles modified by amino-functionalized ionic liquid via dialdehyde starch for phenolic compounds biodegradation. Chem Eng J 391:123564. https://doi.org/10.1016/j.cej.2019.123564
Radjenović J, Petrović M, Barceló D (2009) Fate and distribution of pharmaceuticals in wastewater and sewage sludge of the conventional activated sludge (CAS) and advanced membrane bioreactor (MBR) treatment. Water Res 43:831–841. https://doi.org/10.1016/j.watres.2008.11.043
Shanmugam S, Krishnaswamy S, Chandrababu R, Veerabagu U, Pugazhendhi A, Mathimani T (2020) Optimal immobilization of Trichoderma asperellum laccase on polymer coated Fe3O4@ SiO2 nanoparticles for enhanced biohydrogen production from delignified lignocellulosic biomass. Fuel 273:117777. https://doi.org/10.1016/j.fuel.2020.117777
Shokri Z, Seidi F, Karami S, Li C, Saeb MR, Xiao H (2021) Laccase immobilization onto natural polysaccharides for biosensing and biodegradation. Carbohydr Polym 262:117963. https://doi.org/10.1016/j.carbpol.2021.117963
Sirisha VL, Jain A, Jain A (2016) Enzyme immobilization: an overview on methods, support material, and applications of immobilized enzymes. Adv Food Nutr Res 79:179–211. https://doi.org/10.1016/bs.afnr.2016.07.004
Teerapatsakul C, Parra R, Keshavarz T, Chitradon L (2017) Repeated batch for dye degradation in an airlift bioreactor by laccase entrapped in copper alginate. Biodegradation 120:52–57. https://doi.org/10.1016/j.ibiod.2017.02.001
Thangaraj B, Jia Z, Dai L, Liu D, Du W (2019) Effect of silica coating on Fe3O4 magnetic nanoparticles for lipase immobilization and their application for biodiesel production. Arab J Chem 12:4694–4706. https://doi.org/10.1016/J.ARABJC.2016.09.004
Vaidyanath S, Harish BS, Gayathri G, Trilokesh C, Uppuluri KB, Anbazhagan V (2020) Maximizing the direct recovery and stabilization of cellulolytic enzymes from Trichoderma harzanium BPGF1 fermented broth using carboxymethyl inulin nanoparticles. Int J Biol Macromol 160:964–970. https://doi.org/10.1016/j.ijbiomac.2020.05.185
Vojdanitalab K, Jafari-Nodoushan H, Mojtabavi S, Shokri M, Jahandar H, Faramarzi MA (2022) Instantaneous synthesis and full characterization organic-inorganic laccase-cobalt phosphate hybrid nanoflowers. Sci Rep 12:1–6. https://doi.org/10.1038/s41598-022-13490-w
Wei Y, Han B, Hu X, Lin Y, Wang X, Deng X (2012) Synthesis of Fe3O4 nanoparticles and their magnetic properties. Procedia Eng 27:632–637. https://doi.org/10.1016/j.proeng.2011.12.498
Yang X, Chen Y, Yao S, Qian J, Guo H, Cai X (2019) Preparation of immobilized lipase on magnetic nanoparticles dialdehyde starch. Carbohydr Polym 218:324–332. https://doi.org/10.1016/J.CARBPOL.2019.05.012
Yin QF, Ju BZ, Zhang SF, Wang XB, Yang JZ (2008) Preparation and characteristics of novel dialdehyde aminothiazole starch and its adsorption properties for Cu (II) ions from aqueous solution. Carbohydr Polym 72:326–333. https://doi.org/10.1016/j.carbpol.2007.08.019
Acknowledgements
This work was financially supported by the Grant No. 1400-1-151-52987 from Biotechnology Research Center, Tehran University of Medical Sciences, Tehran, Iran to M.A.F.
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MS: Conceptualization, Methodology, Investigation, and Writing—Original Draft. SM: Data curation, Writing- Original draft preparation, Visualization, and Software. HJ-N: Formal analysis, Writing—Review & Editing, and Conceptualization. KV: Visualization, Investigation, and Methodology. SG: Formal analysis, Investigation, and Methodology. HJ: Software, Validation, and Investigation. MAF: Supervision, Conceptualization, Methodology, Resources, Data Curation, Writing—Review & Editing, Project administration, and Funding acquisition
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Shokri, M., Mojtabavi, S., Jafari-Nodoushan, H. et al. Laccase-loaded magnetic dialdehyde inulin nanoparticles as an efficient heterogeneous natural polymer-based biocatalyst for removal and detoxification of ofloxacin. Biodegradation 33, 489–508 (2022). https://doi.org/10.1007/s10532-022-09994-x
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DOI: https://doi.org/10.1007/s10532-022-09994-x