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

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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.

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References

  1. Wu S, Snajdrova R, Moore J C, Baldenius K, Bornscheuer U T. Biocatalysis: enzymatic synthesis for industrial applications. Angewandte Chemie International Edition, 2021, 60(1): 88–119

    Article  CAS  PubMed  Google Scholar 

  2. Rodrigues R C, Berenguer-Murcia A, Carballares D, Morellon-Sterling R, Fernandez-Lafuente R. Stabilization of enzymes via immobilization: multipoint covalent attachment and other stabilization strategies. Biotechnology Advances, 2021, 52: 107821

    Article  CAS  PubMed  Google Scholar 

  3. Wiltschi B, Cernava T, Dennig A, Galindo Casas M, Geier M, Gruber S, Haberbauer M, Heidinger P, Herrero Acero E, Kratzer R, Luley-Goedl C, Müller C A, Pitzer J, Ribitsch D, Sauer M, Schmölzer K, Schnitzhofer W, Sensen C W, Soh J, Steiner K, Winkler C K, Winkler M, Wriessnegger T. Enzymes revolutionize the bioproduction of value-added compounds: from enzyme discovery to special applications. Biotechnology Advances, 2020, 40: 107520

    Article  CAS  PubMed  Google Scholar 

  4. Jemli S, Ayadi-Zouari D, Hlima H B, Bejar S. Biocatalysts: application and engineering for industrial purposes. Critical Reviews in Biotechnology, 2016, 36(2): 246–258

    Article  CAS  PubMed  Google Scholar 

  5. Bell E L, Finnigan W, France S P, Green A P, Hayes M A, Hepworth L J, Lovelock S L, Niikura H, Osuna S, Romero E, Ryan K S, Turner N J, Flitsch S L. Biocatalysis. Nature Reviews Methods Primers, 2021, 1(1): 46

    Article  CAS  Google Scholar 

  6. Sheldon R A, Pelt S V. Enzyme immobilisation in biocatalysis: why, what and how. Chemical Society Reviews, 2013, 42(15): 6223–6235

    Article  CAS  PubMed  Google Scholar 

  7. Finnigan W, Hepworth L J, Flitsch S L, Turner N J. RetroBioCat as a computer-aided synthesis planning tool for biocatalytic reactions and cascades. Nature Catalysis, 2021, 4(2): 98–104

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Santos A G, da Rocha G O, de Andrade J B. Occurrence of the potent mutagens 2-nitrobenzanthrone and 3-nitrobenzanthrone in fine airborne particles. Scientific Reports, 2019, 9(1): 1–13

    Article  PubMed  PubMed Central  Google Scholar 

  9. Garcia-Galan C, Berenguer-Murcia A, Fernandez-Lafuente R, Rodrigues R C. Potential of different enzyme immobilization strategies to improve enzyme performance. Advanced Synthesis & Catalysis, 2011, 353(16): 2885–2904

    Article  CAS  Google Scholar 

  10. Sheldon R A, Basso A, Brady D. New frontiers in enzyme immobilisation: robust biocatalysts for a circular bio-based economy. Chemical Society Reviews, 2021, 50(10): 5850–5862

    Article  CAS  PubMed  Google Scholar 

  11. Wu X, Hou M, Ge J. Meta-organic frameworks and inorganic nanoflowers: a type of emerging inorganic crystal nanocarrier for enzyme immobilization. Catalysis Science & Technology, 2015, 5(12): 5077–5085

    Article  CAS  Google Scholar 

  12. Cui J, Ren S, Sun B, Jia S. Optimization protocols and improved strategies for metal-organic frameworks for immobilizing enzymes: current development and future challenges. Coordination Chemistry Reviews, 2018, 370: 22–41

    Article  CAS  Google Scholar 

  13. Liu J, Liang J, Xue J, Liang K. Metal-organic frameworks as a versatile materials platform for unlocking new potentials in biocatalysis. Small, 2021, 17(32): e2100300

    Article  PubMed  Google Scholar 

  14. Wang X, Lan P, Ma S. Metal-organic frameworks for enzyme immobilization: beyond host matrix materials. ACS Central Science, 2020, 6(9): 1497–1506

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Gkaniatsou E, Sicard C, Ricoux R, Mahy J P, Steunou N, Serre C. Metal-organic frameworks: a novel host platform for enzymatic catalysis and detection. Materials Horizons, 2017, 4(1): 55–63

    Article  CAS  Google Scholar 

  16. Liang K, Ricco R, Doherty C M, Styles M J, Bell S, Kirby N, Mudie S, Haylock D, Hill A J, Doonan C J, Falcaro P. Biomimetic mineralization of metal-organic frameworks as protective coatings for biomacromolecules. Nature Communications, 2015, 6(1): 7240

    Article  CAS  PubMed  Google Scholar 

  17. Huang W, Zhang W, Gan Y, Yang J, Zhang S. 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

    Google Scholar 

  18. Tong L, Huang S, Shen Y, Liu S, Ma X, Zhu F, Chen G, Ouyang G. Atomically unveiling the structure-activity relationship of biomacromolecule-metal-organic frameworks symbiotic crystal. Nature Communications, 2022, 13(1): 951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Huang S, Chen G, Ouyang G. Confining enzymes in porous organic frameworks: from synthetic strategy and characterization to healthcare applications. Chemical Society Reviews, 2022, 51(15): 6824–6863

    Article  CAS  PubMed  Google Scholar 

  20. Li Z, Wang L, Qin L, Lai C, Wang Z, Zhou M, Xiao L, Liu S, Zhang M. Recent advances in the application of water-stable metal-organic frameworks: adsorption and photocatalytic reduction of heavy metal in water. Chemosphere, 2021, 285: 131432

    Article  CAS  PubMed  Google Scholar 

  21. He T, Kong X J, Li J R. Chemically stable metal-organic frameworks: rational construction and application expansion. Accounts of Chemical Research, 2021, 54(15): 3083–3094

    Article  CAS  PubMed  Google Scholar 

  22. Guo Y, Sun Q, Wu F, Dai Y, Chen X. Polyphenol-containing nanoparticles: synthesis, properties, and therapeutic delivery. Advanced Materials, 2021, 33(22): e2007356

    Article  PubMed  Google Scholar 

  23. Lin Z, Zhou J, Cortez-Jugo C, Han Y, Ma Y, Pan S, Hanssen E, Richardson J J, Caruso F. Ordered mesoporous metal-phenolic network particles. Journal of the American Chemical Society, 2020, 142(1): 335–341

    Article  CAS  PubMed  Google Scholar 

  24. Ejima H, Richardson J J, Caruso F. Metal-phenolic networks as a versatile platform to engineer nanomaterials and biointerfaces. Nano Today, 2017, 12: 136–148

    Article  CAS  Google Scholar 

  25. Chen E, Qiu M, Zhang Y, Zhu Y, Liu L, Sun Y, Bu X, Zhang J, Lin Q. Acid and base resistant zirconium polyphenolate-metalloporphyrin scaffolds for efficient CO2 photoreduction. Advanced Materials, 2018, 30(2): 1704388

    Article  Google Scholar 

  26. Ismail M, Bustam M A, Yeong Y F. Gallate-based metal-organic frameworks, a new family of hybrid materials and their applications: a review. Crystals, 2020, 10(11): 1006

    Article  CAS  Google Scholar 

  27. Chiong J A, Zhu J, Bailey J B, Kalaj M, Subramanian R H, Xu W, Cohen S M, Tezcan F A. An exceptionally stable metal-organic framework constructed from chelate-based metal-organic polyhedra. Journal of the American Chemical Society, 2020, 142(15): 6907–6912

    Article  CAS  PubMed  Google Scholar 

  28. Grape E S, Flores J G, Hidalgo T, Martinez-Ahumada E, Gutierrez-Alejandre A, Hautier A, Williams D R, O’Keeffe M, Ohrstrom L, Willhammar T, Horcajada P, Ibarra I A, Inge A K. A robust and biocompatible bismuth ellagate MOF synthesized under green ambient conditions. Journal of the American Chemical Society, 2020, 142(39): 16795–16804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Miller G N. Use of dinitrosaIicyIic acid reagent for determination of reducing sugar. Analytical Chemistry, 1959, 81(3): 426–428

    Article  Google Scholar 

  30. Wang Z, Zeng Z, Wang H, Zeng G, Xu P, Xiao R, Huang D, Chen S, He Y, Zhou C, Cheng M, Qin H. Bismuth-based metal-organic frameworks and their derivatives: opportunities and challenges. Coordination Chemistry Reviews, 2021, 439: 2139052

    Article  Google Scholar 

  31. Yang N, Sun H. Biocoordination chemistry of bismuth: recent advances. Coordination Chemistry Reviews, 2007, 251(17–20): 2354–2366

    Article  CAS  Google Scholar 

  32. Wang L, Wang Y, He R, Zhuang A, Wang X, Zeng J, Hou J. A new nanobiocatalytic system based on allosteric effect with dramatically enhanced enzymatic performance. Journal of the American Chemical Society, 2013, 135(4): 1272–1275

    Article  CAS  PubMed  Google Scholar 

  33. Jiang Z, Chen Y, Xing M, Ji P, Feng W. Fabrication of a fibrous metal-organic framework and simultaneous immobilization of enzymes. ACS Omega, 2020, 5(36): 22708–22718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Good N E, Winget G D, Winter W, Connolly T N, Izawa S, Singh R M. Hydrogen ion buffers for biological research. Biochemistry, 1966, 5(2): 467–477

    Article  CAS  PubMed  Google Scholar 

  35. Colwell K A, Jackson M N, Torres-Gavosto R M, Jawahery S, Vlaisavljevich B, Falkowski J M, Smit B, Weston S C, Long J R. 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

    Article  CAS  PubMed  Google Scholar 

  36. Fogarty W M, Benson C P. Purification and properties of a thermophilic amyloglucosidase from Aspergillus nige. European Journal of Applied Microbiology and Biotechnology, 1983, 18(5): 271–278

    Article  CAS  Google Scholar 

  37. Pan Y, Li Q, Li H, Farmakes J, Ugrinov A, Zhu X, Lai Z, Chen B, Yang Z. A general Ca-MOM platform with enhanced acid-base stability for enzyme biocatalysis. Chem Catalysis, 2021, 1(1): 146–161

    Article  CAS  Google Scholar 

  38. Pan Y, Li H, Farmakes J, Xiao F, Chen B, Ma S, Yang Z. How do enzymes orient when trapped on metal-organic framework (MOF) surfaces? Journal of the American Chemical Society, 2018, 140(47): 16032–16036

    Article  CAS  PubMed  Google Scholar 

  39. Owusu R K, Makhzoum A, Knapp J S. 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

    Article  CAS  Google Scholar 

  40. Pietricola G, Ottone C, Fino D, Tommasi T. Enzymatic reduction of CO2 to formic acid using FDH immobilized on natural zeolite. Journal of CO2 Utilization, 2020, 42: 101343

    Article  CAS  Google Scholar 

  41. Tang Y, Li W, Muhammad Y, Jiang S, Huang M, Zhang H, Zhao Z, Zhao Z. Fabrication of hollow covalent-organic framework microspheres via emulsion-interfacial strategy to enhance laccase immobilization for tetracycline degradation. Chemical Engineering Journal, 2021, 421: 129743

    Article  CAS  Google Scholar 

  42. Patil P D, Yadav G D. Rapid in situ encapsulation of laccase into metal-organic framework support (ZIF-8) under biocompatible conditions. ChemistrySelect, 2018, 3(17): 4669–4675

    Article  CAS  Google Scholar 

  43. de Castro R J S, Ohara A, Nishide T G, Albernaz J R M, Soares M H, Sato H H. 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

    Article  Google Scholar 

  44. Chen G, Kou X, Huang S, Tong L, Shen Y, Zhu W, Zhu F, Ouyang G. Modulating the biofunctionality of metal-organic-framework-encapsulated enzymes through controllable embedding patterns. Angewandte Chemie International Edition, 2020, 59(7): 2867–2874

    Article  CAS  PubMed  Google Scholar 

  45. Maddigan N K, Tarzia A, Huang D M, Sumby C J, Bell S G, Falcaro P, Doonan C J. Protein surface functionalisation as a general strategy for facilitating biomimetic mineralisation of ZIF-8. Chemical Science, 2018, 9(18): 4217–4123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Hsu P H, Chang C C, Wang T H, Lam P K, Wei M Y, Chen C T, Chen C Y, Chou L Y, Shieh F K. 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

    Article  CAS  Google Scholar 

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Acknowledgements

This work was financially supported by the National Natural Science Foundation of China (Grant Nos. 22178083, 22078081 and 21878068), the Natural Science Foundation of Tianjin China (Grant No. 20JCYBJC00530), the Hebei Key Research and Development Project (Grant No. 20372802D), Open Funding Project of the State Key Laboratory of Biocatalysis and Enzyme Engineering (Grant No. SKLBEE2020011), Science Technology Research Project of Higher Education of Hebei Province (Grant No. QN2021045) and Tianjin Enterprise Science and Technology Commissioner Project (Grant No. 21YDTPJC00810).

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Authors and Affiliations

  1. School of Chemical Engineering and Technology, Hebei University of Technology, Tianjin, 300130, China

    Junyang Xu, Guanhua Liu, Ying He, Liya Zhou, Li Ma, Yunting Liu, Xiaobing Zheng, Jing Gao & Yanjun Jiang

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

    Guanhua Liu, Xiaobing Zheng & Yanjun Jiang

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  1. Junyang Xu
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  2. Guanhua Liu
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  3. Ying He
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  4. Liya Zhou
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  5. Li Ma
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  6. Yunting Liu
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  7. Xiaobing Zheng
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  9. Yanjun Jiang
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Correspondence to Ying He or Yanjun Jiang.

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Xu, J., Liu, G., He, Y. et al. Enzyme@bismuth-ellagic acid: a versatile platform for enzyme immobilization with enhanced acid-base stability. Front. Chem. Sci. Eng. 17, 784–794 (2023). https://doi.org/10.1007/s11705-022-2278-4

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  • DOI: https://doi.org/10.1007/s11705-022-2278-4

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