Skip to main content

Soybean peroxidase immobilized on δ-FeOOH as new magnetically recyclable biocatalyst for removal of ferulic acid

Abstract

A significant enhancement in the catalytic performance due to enzymes immobilization is a great way to enhance the economics of biocatalytic processes. The soybean peroxidase (SP) immobilization under ferroxyte and the ferulic acid removal by the enzyme free and immobilized were investigated. The immobilization via silica-coated ferroxyte nanoparticles was effective, and immobilization yield of 39%. The scanning electron microscopy (SEM) images showed significant changes in the materials morphology. Substantial differences were observed in the particles’ Fourier Transform Infrared (FTIR) spectra. The magnetic catalyst revealed a better performance than the free enzyme in the ferulic acid conversion, presenting a good V max/K m ratio when compared with the free enzyme. The reuse evaluated by ten cycles exhibited excellent recycling, remaining constant between the sixth and seventh cycles. The use of magnetic nanocatalyst becomes possible to eliminate the high operational costs, and complicated steps of the conventional enzymatic processes. Thus, a viable industrial route for the use of the enzyme as catalyst is possible.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  1. 1.

    Yadav BR, Garg A (2013) Ferulic acid degradation by wet oxidation process. Int J ChemTech Res 5:654–658

    CAS  Google Scholar 

  2. 2.

    Santos SA, Rodríguez FP, Romero A (2016) Use of Fenton reagent combined with humic acids for the removal of PFOA from contaminated water. Sci Total Environ 563:657–663. Doi:10.1016/j.scitotenv.2015.09.044

    Article  Google Scholar 

  3. 3.

    Silva MC, Torres JA, Castro AA, Da Cunha EFF, De Oliveira LCA, Corrêa AD, Ramalho TC (2015) Combined experimental and theoretical study on the removal of pollutant compounds by peroxidases: affinity and reactivity toward a bioremediation catalyst. J Biomol Struct Dyn 34:1839–1848. Doi:10.1080/07391102.2015.1063456

    Article  Google Scholar 

  4. 4.

    Ellouze S, Panizza M, Barbucci A, Cerisola G, Mhiri T, Elaoud SC (2016) Ferulic acid treatment by electrochemical oxidation using a BDD anode. J Taiwan Inst Chem Eng 59:132–137. Doi:10.1016/j.jtice.2015.09.008

    CAS  Article  Google Scholar 

  5. 5.

    Diao M, Ouédraogo N, Baba-Moussa L, Savadogo PW, N’Guessan AG, Bassolé IH, Dicko MH (2011) Biodepollution of wastewater containing phenolic compounds from leather industry by plant peroxidases. Biodegradation 2:389–396. doi:10.1007/s10532-010-9410-8

    Article  Google Scholar 

  6. 6.

    Xie XG, Dai CC (2015) Degradation of a model pollutant ferulic acid by the endophytic fungus Phomopsis liquidambari. Bioresour Technol 179:35–42. doi:10.1016/j.biortech.2014.11.112

    CAS  Article  Google Scholar 

  7. 7.

    Mendonça E, Martins A, Anselmo AM (2004) Biodegradation of natural phenolic compounds as single and mixed substrates by Fusarium flocciferum. Electron J Biotechnol 7:38–46

    Article  Google Scholar 

  8. 8.

    Di Paola A, Bellardita M, Megna B, Parrino F, Palmisano L (2015) Photocatalytic oxidation of trans-ferulic acid to vanillin on TiO2 and WO3-loaded TiO2 catalysts. Catal Today 252:195–200. doi:10.1016/j.cattod.2014.09.012

    Article  Google Scholar 

  9. 9.

    Matto M, Husain Q (2009) Calcium alginate-starch hybrid support for both surface immobilization and entrapment of bitter gourd (Momordica charantia) peroxidase. J Mol Catal B Enzym 57:164–170. doi:10.1016/j.molcatb.2008.08.011

    CAS  Article  Google Scholar 

  10. 10.

    Arriel Torres J, Batista Chagas PM, Cristina Silva M, Dos Santos CD, Duarte Corrêa A (2016) Enzymatic oxidation of phenolic compounds in coffee processing wastewater. Water Sci Technol 73:39–50. doi:10.2166/wst.2015.332

    Article  Google Scholar 

  11. 11.

    Nicell JA (1994) Kinetics of horseradish peroxidase-catalysed polymerization and precipitation of aqueous 4-chlorophenol. J Chem Technol Biot 2:203–215

    Article  Google Scholar 

  12. 12.

    Li L, Zeng C, Ai L, Jiang J (2015) Synthesis of reduced graphene oxide-iron nanoparticles with superior enzyme-mimetic activity for biosensing application. J Alloys Compd 639:470–477. doi:10.1016/j.jallcom.2015.03.176

    CAS  Article  Google Scholar 

  13. 13.

    DiCosimo R, McAuliffe J, Poulose AJ, Bohlmann G (2013) Industrial use of immobilized enzymes. Chem Soc Rev 42:6437–6474. doi:10.1039/c3cs35506c

    CAS  Article  Google Scholar 

  14. 14.

    Zuo X, Peng C, Huang Q, Song S, Wang L, Li D, Fan C (2009) Design of a carbon nanotube/magnetic nanoparticle-based peroxidase-like nanocomplex and its application for highly efficient catalytic oxidation of phenols. Nano Res 2:617–623. doi:10.1007/s12274-009-9062-3

    CAS  Article  Google Scholar 

  15. 15.

    Cheng J, Ming Yu S, Zuo P (2006) Horseradish peroxidase immobilized on aluminum-pillared interlayered clay for the catalytic oxidation of phenolic wastewater. Water Res 40:283–290. doi:10.1016/j.watres.2005.11.017

    CAS  Article  Google Scholar 

  16. 16.

    Chen X, Zhao T, Zou J (2009) A novel mimetic peroxidase catalyst by using magnetite-containing silica nanoparticles as carriers. Microchim Acta 164:93–99. doi:10.1007/s00604-008-0038-x

    CAS  Article  Google Scholar 

  17. 17.

    Ma M, Xie J, Zhang Y, Chen Z, Gu N (2013) Fe3O4@Pt nanoparticles with enhanced peroxidase-like catalytic activity. Mater Lett 105:36–39

    CAS  Article  Google Scholar 

  18. 18.

    Chang Q, Jiang GD, Tang HQ, Li N, Huang J, Wu LY (2015) Enzymatic removal of chlorophenols using horseradish peroxidase immobilized on superparamagnetic Fe3O4/graphene oxide nanocomposite. Chin J Catal 36:961–968. doi:10.1016/S1872-2067(15)60856-7

    CAS  Article  Google Scholar 

  19. 19.

    Cao Y, Wen L, Svec F, Tan T, Lv Y (2016) Magnetic AuNP@Fe3O4 nanoparticles as reusable carriers for reversible enzyme immobilization. Chem Eng J 286:272–281. doi:10.1016/j.cej.2015.10.075

    CAS  Article  Google Scholar 

  20. 20.

    Xie W, Zang X (2017) Covalent immobilization of lipase onto aminopropyl-functionalized hydroxyapatite-encapsulated-γ-Fe2O3 nanoparticles: a magnetic biocatalyst for interesterification of soybean oil. Food Chem 227:397–403. doi:10.1016/j.foodchem.2017.01.082

    CAS  Article  Google Scholar 

  21. 21.

    Xie W, Zang X (2016) Immobilized lipase on core–shell structured Fe3O4-MCM-41 nanocomposites as a magnetically recyclable biocatalyst for interesterification of soybean oil and lard. Food Chem 194:1283–1292. doi:10.1016/j.foodchem.2015.09.009

    CAS  Article  Google Scholar 

  22. 22.

    Xie W, Wang J (2014) Enzymatic production of biodiesel from soybean oil by using immobilized lipase on Fe3O4 /poly(styrene-methacrylic acid) magnetic microsphere as a biocatalyst. Energy Fuels 28:2624–2631. doi:10.1021/ef500131s

    CAS  Article  Google Scholar 

  23. 23.

    Xie W, Wang J (2012) Immobilized lipase on magnetic chitosan microspheres for transesterification of soybean oil. Biomass Bioenergy 36:373–380. doi:10.1016/j.biombioe.2011.11.006

    CAS  Article  Google Scholar 

  24. 24.

    Chagas P, Da Silva AC, Passamani EC, Ardisson JD, De Oliveira LCA, Fabris JD, Paniago RM, Monteiro DS, Pereira MC (2013) FeOOH: a superparamagnetic material for controlled heat release under AC magnetic field. J Nanoparticle Res 15:1544. doi:10.1007/s11051-013-1544-2

    Article  Google Scholar 

  25. 25.

    Pereira MC, Garcia EM, Da Silva AC, Lorençon E, Ardisson JD, Murad E, Fabris JD, Matencio T, De Castro TR, Rocha MVJ (2011) Nanostructured δ-FeOOH: a novel photocatalyst for water splitting. J Mat Chem 21:10238–10242. doi:10.1039/c1jm11736j

    Article  Google Scholar 

  26. 26.

    Corrêa S, Lacerda LCT, Pires S, Rocha MVJ, Nogueira FG, Da Silva AC, Pereira MC, De Brito ADB, Da Cunha EF, Ramalho TC (2016) Synthesis, structural characterization and thermal properties of the poly (methylmethacrylate)/δ-FeOOH hybrid material: an experimental and theoretical study. J Nanomater 2016:1–7. doi:10.1155/2016/2462135

    Article  Google Scholar 

  27. 27.

    Gonçalves MA, da Cunha EFF, Peixoto FC, Ramalho TC (2015) Probing thermal and solvent effects on hyperfine interactions and spin relaxation rate of δ-FeOOH (100) and [MnH3buea(OH)]2: toward new MRI probes. Comput Theor Chem 1069:96–104. doi:10.1016/j.comptc.2015.07.006

    Article  Google Scholar 

  28. 28.

    Rocha-Martin J, Velasco-Lozano S, Guisán JM, López-Gallego F (2014) Oxidation of phenolic compounds catalyzed by immobilized multi-enzyme systems with integrated hydrogen peroxide production. Green Chem 16:303–311. doi:10.1039/c3gc41456f

    CAS  Article  Google Scholar 

  29. 29.

    Sharma RK, Dutta S, Sharma S (2015) Quinoline-2-carboimine copper complex immobilized on amine functionalized silica-coated magnetite nanoparticles: a novel and magnetically retrievable catalyst for the synthesis of carbamates via C–H activation of formamides. Dalt Trans 44:1303–1316. doi:10.1039/C4DT03236E

    CAS  Article  Google Scholar 

  30. 30.

    Zhang Q, Han X, Tang B (2013) Preparation of a magnetically recoverable biocatalyst support on monodisperse Fe3O4 nanoparticles. RSC Adv 3:9924–9931. doi:10.1039/c3ra40192h

    CAS  Article  Google Scholar 

  31. 31.

    Gómez A, Bódalo E, Gómez J, Bastida AM, Hidalgo MG (2006) Immobilization of peroxidases on glass beads: an improved alternative for phenol removal. Enzyme Micro Tech 39:1016–1022. doi:10.1016/j.enzmictec.2006.02.008

    Article  Google Scholar 

  32. 32.

    Chang Q, Tang H (2014) Immobilization of horseradish peroxidase on NH2-modified magnetic Fe3O4/SiO2 particles and its application in removal of 2,4-dichlorophenol. Molecules 19:15768–15782. doi:10.3390/molecules191015768

    CAS  Article  Google Scholar 

  33. 33.

    Khan AA, Robinson DS (1994) Hydrogen donor specificity of mango isoperoxidases. Food Chem 49:407–410 doi:10.1016/0308-8146(94)90013-2

    CAS  Article  Google Scholar 

  34. 34.

    Silva M, Torres J, Nogueira F, Tavares T. Corrêa AD, Oliveira LC, Ramalho TC (2016) Immobilization of soybean peroxidase on silica-coated magnetic particles: a magnetically recoverable biocatalyst for pollutant removal. RSC Adv 6:83856–83863

    CAS  Article  Google Scholar 

  35. 35.

    Latimer Junior GW (2012) Association of official analytical chemists-AOAC. Official methods of analysis, 19th edn

  36. 36.

    Barbosa EF, Molina FJ, Lopes FM, García-Ruíz PA, Caramori SS, Fernandes KF (2012) Immobilization of peroxidase onto magnetite modified polyaniline. Sci World J 2012:716374. doi:10.1100/2012/716374

    Google Scholar 

  37. 37.

    Es I, Vieira JDG, Amaral AC (2015) Principles, techniques, and applications of biocatalyst immobilization for industrial application. Appl Microbiol Biotechnol 99:2065–2082. doi:10.1007/s00253-015-6390-y

    CAS  Article  Google Scholar 

  38. 38.

    Matveeva OV, Lakina NV, Doluda VY, Shkileva IP, Matveeva VG, Sulman EM (2015) Effect of peroxidase immobilization on the activity of biocatalysts in trimethylphenol oxidation. Catal Ind 7:161–169. doi:10.1134/S2070050415020063

    Article  Google Scholar 

  39. 39.

    Khoshnevisan K, Bordbar A-K, Zare D, Davoodi D, Noruzi M, Barkhi M, Tabatabaei M (2011) Immobilization of cellulase enzyme on superparamagnetic nanoparticles and determination of its activity and stability. Chem Eng J 171:669–673. doi:10.1016/j.cej.2011.04.039

    CAS  Article  Google Scholar 

  40. 40.

    Fang G, Chen H, Zhang Y, Chen A (2016) Immobilization of pectinase onto Fe3O4@SiO2–NH2 and its activity and stability. Int J Biol Macromol 88:189–195. doi:10.1016/j.ijbiomac.2016.03.059

    CAS  Article  Google Scholar 

  41. 41.

    Klung HP, Alexander LE (1962) X-ray diffraction procedures. Willey, New York

    Google Scholar 

  42. 42.

    Yamaura M, Camilo RL, Sampaio LC, Macedo MA, Nakamura M, Toma HE (2004) Preparation and characterization of (3-aminopropyl) triethoxysilane-coated magnetite nanoparticles. J Magn Magn Mater 279:210–217. doi:10.1016/j.jmmm.2004.01.094

    CAS  Article  Google Scholar 

  43. 43.

    Kahani SA, Jafari M (2009) A new method for preparation of magnetite from iron oxyhydroxide or iron oxide and ferrous salt in aqueous solution. J Magn Magn Mater 321:1951–1954. doi:10.1016/j.jmmm.2008.12.026

    CAS  Article  Google Scholar 

  44. 44.

    Bruni S, Cariati F, Casu M, Lai A, Musinu A (1999) IR and NMR study of nanoparticle-support interactions in a Fe2O3–SiO2 nanocomposite prepared by a Sol–gel method. Nanostructured 11:573–586

    CAS  Article  Google Scholar 

  45. 45.

    Chanéac C, Tronc E, Jolivet J (1996) Magnetic iron oxide–silica nanocomposites. Synthesis and characterization. J Mater Chem 6:1905–1911

    Article  Google Scholar 

  46. 46.

    Buchanan ID, Nicell JA (1998) Kinetics of peroxidase interactions in the presence of a protective additive. J Chem Technol Biot 1:23–32

    Article  Google Scholar 

  47. 47.

    Ansari SA, Husain Q (2012) Potential applications of enzymes immobilized on/in nano materials: a review. Biotech adv 3:512–523

    Article  Google Scholar 

  48. 48.

    Xie T, Wang A, Huang L, Li H, Chen Z, Wang Q, Yin X (2009) Recent advance in the support and technology used in enzyme immobilization. Afr J Biotechnol 8:4724–4733

    CAS  Google Scholar 

  49. 49.

    Guzik U, Hupert-Kocurek K, Wojcieszyńska D (2014) Immobilization as a strategy for improving enzyme properties-application to oxidoreductases. Molecules 19:8995–9018. doi:10.3390/molecules19078995

    Article  Google Scholar 

  50. 50.

    Zhu H, Hu Y, Jiang G, Shen G (2011) Peroxidase-like activity of aminopropyltriethoxysilane-modified iron oxide magnetic nanoparticles and its application to clenbuterol detection. Eur Food Res Technol 233:881–887. doi:10.1007/s00217-011-1582-x

    CAS  Article  Google Scholar 

  51. 51.

    Nicell JA, Bewtra JK, Biswas N, St. Pierre CC, Taylor KE (1993) Enzyme catalyzed polymerization and precipitation of aromatic compounds from aqueous solution. Can J Civ Eng 20:725–735. doi:10.1139/l93-097

    Article  Google Scholar 

  52. 52.

    Long J, Li X, Wu Z, Xu E, Xu X, Jin Z, Jiao A (2015) Immobilization of pullulanase onto activated magnetic chitosan/Fe3O4 nanoparticles prepared by in situ mineralization and effect of surface functional groups on the. Colloids Surf A 472:69–77

    CAS  Article  Google Scholar 

  53. 53.

    Ding S, Cargill AA, Medintz IL, Claussen JC (2015) Increasing the activity of immobilized enzymes with nanoparticle conjugation. Curr Opin Biotechnol 34:242–250. doi:10.1016/j.copbio.2015.04.005

    CAS  Article  Google Scholar 

  54. 54.

    Wu Z, Zhang B, Yan B (2009) Regulation of enzyme activity through interactions with nanoparticles. I J Mol Sci 10:4198–4209. doi:10.3390/ijms10104198

    CAS  Article  Google Scholar 

  55. 55.

    Ardao I, Comenge J, Benaiges MD, Álvaro G, Puntes VF (2012) Rational nanoconjugation improves biocatalytic performance of enzymes: aldol addition catalyzed by immobilized rhamnulose-1-phosphate aldolase. Langmuir 28:6461–6467. doi:10.1021/la3003993

    CAS  Article  Google Scholar 

  56. 56.

    Pandey P, Singh SP, Arya SK, Gupta V, Datta M, Singh S, Malhotra BD (2007) Application of thiolated gold nanoparticles for the enhancement of glucose oxidase activity. Langmuir 23:3333–3337. doi:10.1021/la062901c

    CAS  Article  Google Scholar 

  57. 57.

    Karim Z, Adnan R, Ansari MS (2012) Low concentration of silver nanoparticles not only enhances the activity of horseradish peroxidase but alter the structure also. PLoS One 7:e41422. doi:10.1371/journal.pone.0041422

    CAS  Article  Google Scholar 

  58. 58.

    Kim S, Lee J, Jang S, Lee H, Sung D, Chang JH (2016) High efficient chromogenic catalysis of tetramethylbenzidine with horseradish peroxidase immobilized magnetic nanoparticles. Biochem Eng J 105:406–411. doi:10.1016/j.bej.2015.10.019

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors thank the Brazilian agencies FAPEMIG, CAPES, and CNPq for the financial support of this research, and UFLA for infrastructure and encouragement in this work. This work was also supported by the Excellence project FIM.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Teodorico C. Ramalho.

Ethics declarations

Conflict of interest

The respective authors certify that they have no affiliations with or involvement in any organization or entity with any financial interest (such as honoraria; membership, employment, consultancies or patent-licensing arrangements), or non-financial interest (such as personal, affiliations, or beliefs) in the subject matter or materials discussed in this manuscript.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Tavares, T.S., Torres, J.A., Silva, M.C. et al. Soybean peroxidase immobilized on δ-FeOOH as new magnetically recyclable biocatalyst for removal of ferulic acid. Bioprocess Biosyst Eng 41, 97–106 (2018). https://doi.org/10.1007/s00449-017-1848-1

Download citation

Keywords

  • Biocatalyst
  • Iron oxide
  • Bioremediation
  • Wastewater