Enzyme@bismuth-ellagic acid: a versatile platform for enzyme immobilization with enhanced acid-base stability

doi:10.1007/s11705-022-2278-4

Front. Chem. Sci. Eng.

2023, Vol. 17

Issue (6) : 784-794 https://doi.org/10.1007/s11705-022-2278-4

RESEARCH ARTICLE

Enzyme@bismuth-ellagic acid: a versatile platform for enzyme immobilization with enhanced acid-base stability

Junyang Xu¹, Guanhua Liu^1,², Ying He¹(

), Liya Zhou¹, Li Ma¹, Yunting Liu¹, Xiaobing Zheng^1,², Jing Gao¹, Yanjun Jiang^1,²(

)

¹. School of Chemical Engineering and Technology, Hebei University of Technology, Tianjin 300130, China
². National-Local Joint Engineering Laboratory for Energy Conservation of Chemical Process Integration and Resources Utilization, Hebei University of Technology, Tianjin 300130, China

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Abstract

In situ encapsulation is an effective way to synthesize enzyme@metal–organic framework biocatalysts; however, it is limited by the conditions of metal–organic framework synthesis and its acid-base stability. Herein, a biocatalytic platform with improved acid-base stability was constructed via a one-pot method using bismuth-ellagic acid as the carrier. Bismuth-ellagic acid is a green phenol-based metal–organic framework whose organic precursor is extracted from natural plants. After encapsulation, the stability, especially the acid-base stability, of amyloglucosidases@bismuth-ellagic acid was enhanced, which remained stable over a wide pH range (2–12) and achieved multiple recycling. By selecting a suitable buffer, bismuth-ellagic acid can encapsulate different types of enzymes and enable interactions between the encapsulated enzymes and cofactors, as well as between multiple enzymes. The green precursor, simple and convenient preparation process provided a versatile strategy for enzymes encapsulation.

Keywords bismuth-ellagic acid in situ encapsulation enzyme@MOF biocomposites

Corresponding Author(s): Ying He,Yanjun Jiang

Online First Date: 31 March 2023 Issue Date: 17 May 2023

Cite this article:

Junyang Xu,Guanhua Liu,Ying He, et al. Enzyme@bismuth-ellagic acid: a versatile platform for enzyme immobilization with enhanced acid-base stability[J]. Front. Chem. Sci. Eng., 2023, 17(6): 784-794.

URL:

https://academic.hep.com.cn/fcse/EN/10.1007/s11705-022-2278-4
https://academic.hep.com.cn/fcse/EN/Y2023/V17/I6/784

Fig.1 (a) PXRD patterns and SEM images of (b) Bi-EA-3, (c) Bi-EA-4, (d) Bi-EA-5, (e) Bi-EA-6 and (f) Bi-EA-7.

Fig.2 Characterization of AMG@Bi-EA: (a) SEM image of AMG@Bi-EA; (b) laser confocal image of AMG@Bi-EA; (c) XRD pattern of AMG@Bi-EA with the addition of different AMG; (d) thermogravimetric analysis (TGA) curves of enzyme@Bi-EA and Bi-EA; (e) nitrogen adsorption and desorption isotherms of AMG@Bi-EA and Bi-EA; (f) their corresponding pore size distribution.

Fig.3 (a) The catalytic activity and (b) enzymatic kinetics analysis of free amyloglucosidase and AMG@Bi-EA.

Tab.1 Kinetic parameters of free AMG and AMG@Bi-EA

Fig.4 (a) Turbidity and (b) XRD analysis of AMG@Bi-EA after immersion in buffers of different pH; (c) the activity of AMG@Bi-EA after immersion in buffers of different pH and (d) its stability in a weakly acidic solution in the presence of proteases.

Tab.2 Thermal deactivation kinetic parameters of free AMG and AMG@Bi-EA

Fig.5 (a, b) Thermal stability, (c, d) thermal inactivation kinetic studies and (e, f) Arrhenius plot for the inactivation of free AMG and AMG@Bi-EA.

Fig.6 (a) The reusability and (b) storage stability of AMG@Bi-EA.

1	S Wu, R Snajdrova, J C Moore, K Baldenius, U T Bornscheuer. Biocatalysis: enzymatic synthesis for industrial applications. Angewandte Chemie International Edition, 2021, 60(1): 88–119 https://doi.org/10.1002/anie.202006648
2	R C Rodrigues, A Berenguer-Murcia, D Carballares, R Morellon-Sterling, R Fernandez-Lafuente. Stabilization of enzymes via immobilization: multipoint covalent attachment and other stabilization strategies. Biotechnology Advances, 2021, 52: 107821 https://doi.org/10.1016/j.biotechadv.2021.107821
3	B Wiltschi, T Cernava, A Dennig, Casas M Galindo, M Geier, S Gruber, M Haberbauer, P Heidinger, Acero E Herrero, R Kratzer, C Luley-Goedl, C A Müller, J Pitzer, D Ribitsch, M Sauer, K Schmölzer, W Schnitzhofer, C W Sensen, J Soh, K Steiner, C K Winkler, M Winkler, T Wriessnegger. Enzymes revolutionize the bioproduction of value-added compounds: from enzyme discovery to special applications. Biotechnology Advances, 2020, 40: 107520 https://doi.org/10.1016/j.biotechadv.2020.107520
4	S Jemli, D Ayadi-Zouari, H B Hlima, S Bejar. Biocatalysts: application and engineering for industrial purposes. Critical Reviews in Biotechnology, 2016, 36(2): 246–258 https://doi.org/10.3109/07388551.2014.950550
5	E L Bell, W Finnigan, S P France, A P Green, M A Hayes, L J Hepworth, S L Lovelock, H Niikura, S Osuna, E Romero, K S Ryan, N J Turner, S L Flitsch. Biocatalysis. Nature Reviews Methods Primers, 2021, 1(1): 46 https://doi.org/10.1038/s43586-021-00044-z
6	R A Sheldon, S V Pelt. Enzyme immobilisation in biocatalysis: why, what and how. Chemical Society Reviews, 2013, 42(15): 6223–6235 https://doi.org/10.1039/C3CS60075K
7	W Finnigan, L J Hepworth, S L Flitsch, N J Turner. RetroBioCat as a computer-aided synthesis planning tool for biocatalytic reactions and cascades. Nature Catalysis, 2021, 4(2): 98–104 https://doi.org/10.1038/s41929-020-00556-z
8	A G Santos, G O da Rocha, J B de Andrade. Occurrence of the potent mutagens 2-nitrobenzanthrone and 3-nitrobenzanthrone in fine airborne particles. Scientific Reports, 2019, 9(1): 1–13 https://doi.org/10.1038/s41598-018-37186-2
9	C Garcia-Galan, A Berenguer-Murcia, R Fernandez-Lafuente, R C Rodrigues. Potential of different enzyme immobilization strategies to improve enzyme performance. Advanced Synthesis & Catalysis, 2011, 353(16): 2885–2904 https://doi.org/10.1002/adsc.201100534
10	R A Sheldon, A Basso, D Brady. New frontiers in enzyme immobilisation: robust biocatalysts for a circular bio-based economy. Chemical Society Reviews, 2021, 50(10): 5850–5862 https://doi.org/10.1039/D1CS00015B
11	X Wu, M Hou, J Ge. Meta-organic frameworks and inorganic nanoflowers: a type of emerging inorganic crystal nanocarrier for enzyme immobilization. Catalysis Science & Technology, 2015, 5(12): 5077–5085 https://doi.org/10.1039/C5CY01181G
12	J Cui, S Ren, B Sun, S Jia. Optimization protocols and improved strategies for metal–organic frameworks for immobilizing enzymes: current development and future challenges. Coordination Chemistry Reviews, 2018, 370: 22–41 https://doi.org/10.1016/j.ccr.2018.05.004
13	J Liu, J Liang, J Xue, K Liang. Metal–organic frameworks as a versatile materials platform for unlocking new potentials in biocatalysis. Small, 2021, 17(32): e2100300 https://doi.org/10.1002/smll.202100300
14	X Wang, P Lan, S Ma. Metal–organic frameworks for enzyme immobilization: beyond host matrix materials. ACS Central Science, 2020, 6(9): 1497–1506 https://doi.org/10.1021/acscentsci.0c00687
15	E Gkaniatsou, C Sicard, R Ricoux, J P Mahy, N Steunou, C Serre. Metal–organic frameworks: a novel host platform for enzymatic catalysis and detection. Materials Horizons, 2017, 4(1): 55–63 https://doi.org/10.1039/C6MH00312E
16	K Liang, R Ricco, C M Doherty, M J Styles, S Bell, N Kirby, S Mudie, D Haylock, A J Hill, C J Doonan, P Falcaro. Biomimetic mineralization of metal–organic frameworks as protective coatings for biomacromolecules. Nature Communications, 2015, 6(1): 7240 https://doi.org/10.1038/ncomms8240
17	W HuangW ZhangY GanJ YangS Zhang. Laccase immobilization with metal–organic frameworks: current status, remaining challenges and future perspectives. Critical Reviews in Environmental Science and Technology, 2020, 52, 7: 1282–1324
18	L Tong, S Huang, Y Shen, S Liu, X Ma, F Zhu, G Chen, G Ouyang. Atomically unveiling the structure-activity relationship of biomacromolecule-metal–organic frameworks symbiotic crystal. Nature Communications, 2022, 13(1): 951 https://doi.org/10.1038/s41467-022-28615-y
19	S Huang, G Chen, G Ouyang. Confining enzymes in porous organic frameworks: from synthetic strategy and characterization to healthcare applications. Chemical Society Reviews, 2022, 51(15): 6824–6863 https://doi.org/10.1039/D1CS01011E
20	Z Li, L Wang, L Qin, C Lai, Z Wang, M Zhou, L Xiao, S Liu, M Zhang. Recent advances in the application of water-stable metal–organic frameworks: adsorption and photocatalytic reduction of heavy metal in water. Chemosphere, 2021, 285: 131432 https://doi.org/10.1016/j.chemosphere.2021.131432
21	T He, X J Kong, J R Li. Chemically stable metal–organic frameworks: rational construction and application expansion. Accounts of Chemical Research, 2021, 54(15): 3083–3094 https://doi.org/10.1021/acs.accounts.1c00280
22	Y Guo, Q Sun, F Wu, Y Dai, X Chen. Polyphenol-containing nanoparticles: synthesis, properties, and therapeutic delivery. Advanced Materials, 2021, 33(22): e2007356 https://doi.org/10.1002/adma.202007356
23	Z Lin, J Zhou, C Cortez-Jugo, Y Han, Y Ma, S Pan, E Hanssen, J J Richardson, F Caruso. Ordered mesoporous metal-phenolic network particles. Journal of the American Chemical Society, 2020, 142(1): 335–341 https://doi.org/10.1021/jacs.9b10835
24	H Ejima, J J Richardson, F Caruso. Metal-phenolic networks as a versatile platform to engineer nanomaterials and biointerfaces. Nano Today, 2017, 12: 136–148 https://doi.org/10.1016/j.nantod.2016.12.012
25	E Chen, M Qiu, Y Zhang, Y Zhu, L Liu, Y Sun, X Bu, J Zhang, Q Lin. Acid and base resistant zirconium polyphenolate-metalloporphyrin scaffolds for efficient CO2 photoreduction. Advanced Materials, 2018, 30(2): 1704388 https://doi.org/10.1002/adma.201704388
26	M Ismail, M A Bustam, Y F Yeong. Gallate-based metal–organic frameworks, a new family of hybrid materials and their applications: a review. Crystals, 2020, 10(11): 1006 https://doi.org/10.3390/cryst10111006
27	J A Chiong, J Zhu, J B Bailey, M Kalaj, R H Subramanian, W Xu, S M Cohen, F A Tezcan. An exceptionally stable metal–organic framework constructed from chelate-based metal–organic polyhedra. Journal of the American Chemical Society, 2020, 142(15): 6907–6912 https://doi.org/10.1021/jacs.0c01626
28	E S Grape, J G Flores, T Hidalgo, E Martinez-Ahumada, A Gutierrez-Alejandre, A Hautier, D R Williams, M O’Keeffe, L Ohrstrom, T Willhammar, P Horcajada, I A Ibarra, A K Inge. A robust and biocompatible bismuth ellagate MOF synthesized under green ambient conditions. Journal of the American Chemical Society, 2020, 142(39): 16795–16804 https://doi.org/10.1021/jacs.0c07525
29	G N Miller. Use of dinitrosaIicyIic acid reagent for determination of reducing sugar. Analytical Chemistry, 1959, 81(3): 426–428 https://doi.org/10.1021/ac60147a030
30	Z Wang, Z Zeng, H Wang, G Zeng, P Xu, R Xiao, D Huang, S Chen, Y He, C Zhou, M Cheng, H Qin. Bismuth-based metal–organic frameworks and their derivatives: opportunities and challenges. Coordination Chemistry Reviews, 2021, 439: 2139052 https://doi.org/10.1016/j.ccr.2021.213902
31	N Yang, H Sun. Biocoordination chemistry of bismuth: recent advances. Coordination Chemistry Reviews, 2007, 251(17-20): 2354–2366 https://doi.org/10.1016/j.ccr.2007.03.003
32	L Wang, Y Wang, R He, A Zhuang, X Wang, J Zeng, J Hou. A new nanobiocatalytic system based on allosteric effect with dramatically enhanced enzymatic performance. Journal of the American Chemical Society, 2013, 135(4): 1272–1275 https://doi.org/10.1021/ja3120136
33	Z Jiang, Y Chen, M Xing, P Ji, W Feng. Fabrication of a fibrous metal–organic framework and simultaneous immobilization of enzymes. ACS Omega, 2020, 5(36): 22708–22718 https://doi.org/10.1021/acsomega.0c00868
34	N E Good, G D Winget, W Winter, T N Connolly, S Izawa, R M Singh. Hydrogen ion buffers for biological research. Biochemistry, 1966, 5(2): 467–477 https://doi.org/10.1021/bi00866a011
35	K A Colwell, M N Jackson, R M Torres-Gavosto, S Jawahery, B Vlaisavljevich, J M Falkowski, B Smit, S C Weston, J R Long. Buffered coordination modulation as a means of controlling crystal morphology and molecular diffusion in an anisotropic metal–organic framework. Journal of the American Chemical Society, 2021, 143(13): 5044–5052 https://doi.org/10.1021/jacs.1c00136
36	W M Fogarty, C P Benson. Purification and properties of a thermophilic amyloglucosidase from Aspergillus nige. European Journal of Applied Microbiology and Biotechnology, 1983, 18(5): 271–278 https://doi.org/10.1007/BF00500491
37	Y Pan, Q Li, H Li, J Farmakes, A Ugrinov, X Zhu, Z Lai, B Chen, Z Yang. A general Ca-MOM platform with enhanced acid-base stability for enzyme biocatalysis. Chem Catalysis, 2021, 1(1): 146–161 https://doi.org/10.1016/j.checat.2021.03.001
38	Y Pan, H Li, J Farmakes, F Xiao, B Chen, S Ma, Z Yang. How do enzymes orient when trapped on metal–organic framework (MOF) surfaces?. Journal of the American Chemical Society, 2018, 140(47): 16032–16036 https://doi.org/10.1021/jacs.8b09257
39	R K Owusu, A Makhzoum, J S Knapp. Heat inactivation of lipase from psychrotrophic Pseudomonas fluorescens P38: activation parameters and enzyme stability at low or ultra-high temperatures. Food Chemistry, 1992, 44(4): 261–268 https://doi.org/10.1016/0308-8146(92)90048-7
40	G Pietricola, C Ottone, D Fino, T Tommasi. Enzymatic reduction of CO2 to formic acid using FDH immobilized on natural zeolite. Journal of CO2 Utilization, 2020, 42: 101343
41	Y Tang, W Li, Y Muhammad, S Jiang, M Huang, H Zhang, Z Zhao, Z Zhao. Fabrication of hollow covalent-organic framework microspheres via emulsion-interfacial strategy to enhance laccase immobilization for tetracycline degradation. Chemical Engineering Journal, 2021, 421: 129743 https://doi.org/10.1016/j.cej.2021.129743
42	P D Patil, G D Yadav. Rapid in situ encapsulation of laccase into metal–organic framework support (ZIF-8) under biocompatible conditions. ChemistrySelect, 2018, 3(17): 4669–4675 https://doi.org/10.1002/slct.201702852
43	R J S de Castro, A Ohara, T G Nishide, J R M Albernaz, M H Soares, H H Sato. A new approach for proteases production by Aspergillus niger based on the kinetic and thermodynamic parameters of the enzymes obtained. Biocatalysis and Agricultural Biotechnology, 2015, 4(2): 199–207 https://doi.org/10.1016/j.bcab.2014.12.001
44	G Chen, X Kou, S Huang, L Tong, Y Shen, W Zhu, F Zhu, G Ouyang. Modulating the biofunctionality of metal–organic-framework-encapsulated enzymes through controllable embedding patterns. Angewandte Chemie International Edition, 2020, 59(7): 2867–2874 https://doi.org/10.1002/anie.201913231
45	N K Maddigan, A Tarzia, D M Huang, C J Sumby, S G Bell, P Falcaro, C J Doonan. Protein surface functionalisation as a general strategy for facilitating biomimetic mineralisation of ZIF-8. Chemical Science, 2018, 9(18): 4217–4123 https://doi.org/10.1039/C8SC00825F
46	P H Hsu, C C Chang, T H Wang, P K Lam, M Y Wei, C T Chen, C Y Chen, L Y Chou, F K Shieh. Rapid fabrication of biocomposites by encapsulating enzymes into Zn-MOF-74 via a mild water-based approach. ACS Applied Materials & Interfaces, 2021, 13(44): 52014–52022 https://doi.org/10.1021/acsami.1c09052

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