Lysine-modulated synthesis of enzyme-embedded hydrogen-bonded organic frameworks for efficient carbon dioxide fixation

Abstract

Carbonic anhydrase (CA) is an important carbon fixation enzyme. Immobilization of CA can expand its application in the realm of adsorption, catalysis, and so on. As a typical metal-free framework, hydrogen-bonded organic frameworks (HOFs) featuring mild synthesis process, exquisite framework structure and good enzyme compatibility have been used for enzyme embedding. However, the catalytic performance of CA-embedded HOFs (CA@HOFs) is limited by the micropore size of HOFs and the slow adsorption of CO₂. Herein, CA@Lys-HOF-1 was synthesized by introducing lysine (Lys), a basic amino acid, during the coprecipitation of CA and HOFs for CO₂ fixation. The addition of Lys enlarged the average pore size of HOF-1 from 1.8 to 3.2 nm, whereas the introduced -NH₂ groups increased the initial adsorption of CO₂ from 0.55 to 1.21 cm³ g^-1. Compared to CA@HOF-1, the activity of CA@Lys-HOF-1 was enhanced by 71.25%, and the corresponding production of CaCO₃ was enhanced by 12.7%. After eight reaction cycles, CA@Lys-HOF-1 still maintained an output of 9.97 mg of CaCO₃ every 5 min, 83.7% of the initial production. It is hoped that the CA@Lys-HOF-1 reported offers a platform for efficient and continuous fixation of CO₂.

Keywords

Carbon dioxide fixation / carbonic anhydrase / hydrogen-bonded organic frameworks / enzyme catalysis / enzyme immobilization

References

[1] Yaashikaa P,Varjani SJ.A review on photochemical, biochemical and electrochemical transformation of CO₂ into value-added products.J CO2 Util2019;33:131-47

[2] Zhao T,Chen W.Artificial bioconversion of carbon dioxide.Chinese J Catal2019;40:1421-37

[3] Markewitz P,Leitner W.Worldwide innovations in the development of carbon capture technologies and the utilization of CO₂.Energy Environ Sci2012;5:7281

[4] Hermida-Carrera C,Galmés J.Rubisco catalytic properties and temperature response in crops.Plant Physiol2016;171:2549-61 PMCID:PMC4972260

[5] Cummins PL,Gready JE.Directions for optimization of photosynthetic carbon fixation: RuBisCo’s efficiency may not be so constrained after all.Front Plant Sci2018;9:183 PMCID:PMC5838012

[6] Itakura AK,Atkinson N.A Rubisco-binding protein is required for normal pyrenoid number and starch sheath morphology in Chlamydomonas reinhardtii.Proc Natl Acad Sci USA2019;116:18445-54 PMCID:PMC6744930

[7] Valegård K,Haslam RP.Structural and functional analyses of Rubisco from arctic diatom species reveal unusual posttranslational modifications.J Biol Chem2018;293:13033-43 PMCID:PMC6109933

[8] Lindskog S.The catalytic mechanism of carbonic anhydrase..Proc Natl Acad Sci USA1973;70:2505-8

[9] Cao S,Li X.Novel nano-/micro-biocatalyst: soybean epoxide hydrolase immobilized on UiO-66-NH₂ MOF for efficient biosynthesis of enantiopure (R)-1, 2-octanediol in deep eutectic solvents.ACS Sustain Chem Eng2016;4:3586-95

[10] Cao S,Ma Y.Recent advances in immobilized enzymes on nanocarriers.Chinese J Catal2016;37:1814-23

[11] Cao S,Lai L.Magnetic ZIF-8/cellulose/Fe₃O₄ nanocomposite: preparation, characterization, and enzyme immobilization.Bioresour Bioprocess2017;4:1-7

[12] Alizadeh N,Hallaj R,Soleimani F.Ni-hemin metal-organic framework with highly efficient peroxidase catalytic activity: toward colorimetric cancer cell detection and targeted therapeutics.J Nanobiotechnology2018;16:93 PMCID:PMC6245618

[13] Drout RJ,Farha OK.Catalytic applications of enzymes encapsulated in metal-organic frameworks.Coord Chem Rev2019;381:151-60

[14] Wu X,Ge J.Metal-organic frameworks and inorganic nanoflowers: a type of emerging inorganic crystal nanocarrier for enzyme immobilization.Catal Sci Technol2015;5:5077-85

[15] Doonan C,Liang K,Falcaro P.Metal-organic frameworks at the biointerface: synthetic strategies and applications.Acc Chem Res2017;50:1423-32

[16] Riccò R,Li S.Metal-organic frameworks for cell and virus biology: a perspective.ACS Nano2018;12:13-23

[17] Du Y,Zhou L.MOF-based nanotubes to hollow nanospheres through protein-induced soft-templating pathways.Adv Sci (Weinh)2019;6:1801684 PMCID:PMC6425429

[18] Sun Q,Aguila B.Pore environment control and enhanced performance of enzymes infiltrated in covalent organic frameworks.J Am Chem Soc2018;140:984-92

[19] Serre C,Dietzel PD.Introduction to special issue: metal organic frameworks.Microporous Mesoporous Mater2012;157:1-2

[20] Furukawa H,O'Keeffe M.The chemistry and applications of metal-organic frameworks.Science2013;341:1230444

[21] Eum K,Rashidi F.Highly tunable molecular sieving and adsorption properties of mixed-linker zeolitic imidazolate frameworks.J Am Chem Soc2015;137:4191-7

[22] Zhang H,Hu Y.Ultrafast selective transport of alkali metal ions in metal organic frameworks with subnanometer pores.Sci Adv2018;4:eaaq0066 PMCID:PMC5817922

[23] Luo J,Zhang J,Zhong D.Hydrogen-bonded organic frameworks: design, structures and potential applications.CrystEngComm2018;20:5884-98

[24] Lin RB,Li P,Zhou W.Multifunctional porous hydrogen-bonded organic framework materials.Chem Soc Rev2019;48:1362-89

[25] Hisaki I,Takahashi K.Designing hydrogen-bonded organic frameworks (HOFs) with permanent porosity.Angew Chem Int Ed Engl2019;58:11160-70

[26] Luzuriaga MA,Gaertner MW.ZIF-8 degrades in cell media, serum, and some-but not all-common laboratory buffers.Supramol Chem2019;31:485-90

[27] Velásquez-hernández MDJ,Carraro F.Degradation of ZIF-8 in phosphate buffered saline media.CrystEngComm2019;21:4538-44

[28] Luzuriaga MA,Dharmarwardana M.Enhanced Stability and controlled delivery of MOF-encapsulated vaccines and their immunogenic response in vivo.ACS Appl Mater Interf2019;11:9740-6

[29] Sun CY,Wang XL.Zeolitic Imidazolate framework-8 as efficient pH-sensitive drug delivery vehicle.Dalton Trans2012;41:6906-9

[30] Persico F.Use of hydrogen bonds to control molecular aggregation. Behavior of a self-complementary dipyridone designed to self-replicate.J Org Chem1993;58:95-9

[31] Russell VA,Li W.Nanoporous molecular sandwiches: pillared two-dimensional hydrogen-bonded networks with adjustable porosity.Science1997;276:575-9

[32] Tamames-Tabar C,Imbuluzqueta E.Cytotoxicity of nanoscaled metal-organic frameworks.J Mater Chem B2014;2:262-71

[33] Grall R,Delic J,Chevillard S.In vitro biocompatibility of mesoporous metal (III; Fe, Al, Cr) trimesate MOF nanocarriers.J Mater Chem B2015;3:8279-92

[34] Tang Z,Tong L.A biocatalytic cascade in an ultrastable mesoporous hydrogen-bonded organic framework for point-of-care biosensing.Angew Chem Int Ed Engl2021;60:23608-13

[35] Bao Z,Chang G.Fine tuning and specific binding sites with a porous hydrogen-bonded metal-complex framework for gas selective separations.J Am Chem Soc2018;140:4596-603

[36] Tang J,Zheng Q.In-situ encapsulation of protein into nanoscale hydrogen-bonded organic frameworks for intracellular biocatalysis.Angew Chem Int Ed Engl2021;60:22315-21

[37] Liang W,Solomon MB.Enzyme encapsulation in a porous hydrogen-bonded organic framework.J Am Chem Soc2019;141:14298-305

[38] Qin Z,Yang X,Li Y.Heterogenizing homogeneous cocatalysts by well-designed hollow MOF-based nanoreactors for efficient and size-selective CO₂ fixation.Appl Catal B Environ2022;307:121163