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Lamellar Enzyme-Metal–Organic Framework Composites Enable Catalysis on Large Substrates

2021; Chinese Chemical Society; Volume: 4; Issue: 3 Linguagem: Inglês

10.31635/ccschem.021.202000759

2096-5745

Yunjie Tu, Li He, Tao Tu, Qi Zhang,

Dendrimers and Hyperbranched Polymers

Open AccessCCS ChemistryCOMMUNICATION1 Mar 2022Lamellar Enzyme-Metal–Organic Framework Composites Enable Catalysis on Large Substrates Yunjie Tu, He Li, Tao Tu and Qi Zhang Yunjie Tu Department of Chemistry, Fudan University, Shanghai 200433 , He Li Department of Chemistry, Fudan University, Shanghai 200433 , Tao Tu Department of Chemistry, Fudan University, Shanghai 200433 and Qi Zhang *Corresponding author: E-mail Address: [email protected] Department of Chemistry, Fudan University, Shanghai 200433 https://doi.org/10.31635/ccschem.021.202000759 SectionsSupplemental MaterialAboutAbstractPDF ToolsAdd to favoritesDownload CitationsTrack Citations ShareFacebookTwitterLinked InEmail Zeolitic imidazolate framework (ZIF) is a representative type of metal–organic framework that has been extensively used as a carrier in enzyme immobilization. However, thus far the immobilization studies have mainly been carried out on enzymes with small substrates (e.g., peroxide and glucose), and the general applicability of ZIF in enzyme immobilization has not been investigated. In this study, we show that, owing to its small aperture size, the canonical sodalite ZIF [ZIF-8 or sod-Zn(mIM)2 (mIM = 2-methylimidazolate)] cannot be used for enzymes with large substrates. Instead, we show that the lamellar, nanoflower-like ZIF [nf-Zn(mIM)2] synthesized in low precursor concentrations overcomes the size limitation of sod-Zn(mIM)2 and is suitable for immobilization of various enzymes with large substrates. Remarkably, the lamellar ZIF can work with a thioesterase, which acts on a peptide with 11 amino acids to produce an analog of teixobactin, a superantibiotic with no antimicrobial resistance thus far. The lamellar ZIF scaffold is highly efficient in enzyme loading and significantly increases enzyme stability against disfavorable conditions, serving as a general carrier in enzyme immobilization. Download figure Download PowerPoint Introduction Enzyme immobilization is a promising strategy in the application of enzymes as catalysts.1–4 By binding an enzyme to a solid support (carrier), this method provides facile separation, efficient recovery and reuse of enzymes, and increased enzyme lifetime and efficiency under working conditions that are generally far from the cellular environment. Metal–organic frameworks (MOFs) are hybrid porous materials consisting of a regular array of positively charged metal ions surrounded by organic ligands linked through coordination bonds. Owing to many excellent properties such as high surface area, facile tuning of pore size, good chemical and thermal stability, and biocompatibility, MOFs have attracted considerable attention as a promising carrier for enzyme immobilization. During the past decade, a large number of enzyme-MOF composites have been synthesized, and different synthetic approaches have been developed.5–8 To date, the most widely studied MOF for enzyme immobilization is the zeolitic imidazolate framework (ZIF)-8.9–31 ZIF-8 has a sodalite (sod) topology composed of tetrahedral Zn2+ nodes linked via 2-methylimidazolate (mIM) ligands, and hence, is also termed sod-Zn(mIM)2.32,33 Sod-Zn(mIM)2 can be synthesized in aqueous (aq) conditions at room temperature, allowing for facile production of enzyme-MOF composites by simply mixing enzymes with the Zn2+ and mIM precursors. This simple coprecipitation approach enables enzymes to be encapsulated within the sod-Zn(mIM)2 scaffold. The rigid molecular architecture then forms a protective coating around the enzyme, protecting it from external environments that would normally lead to its degradation. Despite the great success of this application, thus far most studies have been performed on model enzymes such as peroxidase, cytochrome c, glucose oxidase, and lipases, all of which act on small substrates.9–29 To extend the use of ZIF as a general carrier in enzyme immobilization, a more extensive survey of different enzymes in this application is necessary. In this study, we show that sod-Zn(mIM)2 is not suitable for enzymes with relatively large substrates such as adenosine triphosphate (ATP) and nicotinamide adenine dinucleotide (NAD+/NADH). Instead, the lamellar, nanoflower-like ZIF produced in low precursor concentrations overcomes the pore size limitation of sod-Zn(mIM)2 and at the same time significantly increases enzyme stability against disfavorable conditions. Results and Discussion In an attempt to expand the use of sod-Zn(mIM)2 in enzyme immobilization, we selected S-adenosylmethionine synthase (SamS) as a model enzyme. SamS converts l-methionine and ATP to S-adenosylmethionine (SAM), the common substrate for all the radical SAM enzymes and most methyltransferases (Figure 1a).34–38 To this end, [email protected](mIM)2 was synthesized according to the previously reported procedures.39 Briefly, the aq solution of SamS and mIM was mixed with Zn(NO3)2 to form a solution in which the final concentrations of SamS, Zn2+, and mIM were about 3 μM, 20 mM, and 1.4 M, respectively. After stirring for 4 h, the resulting enzyme-MOF composite was collected by centrifugation, and then washed three times, respectively, by Tris buffer and sodium dodecyl sulfate (SDS) solution to remove the surface-bound enzyme. Figure 1 | ZIF-based immobilization of SamS. (a) SamS-catalyzed SAM synthesis. (b) SEM analysis of [email protected](mIM)2 (sample 1 in Table 1). (c) PXRD analysis of [email protected](mIM)2 and the simulated spectrum of sod-Zn(MIM)2. (d) SEM analysis of [email protected](mIM)2 (sample 18 in Table 1). (e) PXRD analysis of [email protected](mIM)2. (f) FTIR spectra of nf-Zn(mIM)2 and [email protected](mIM)2. The characteristic absorption bands in the ranges from ∼1640 to 1660 cm−1 and from ∼1510 to 1560 cm−1 correspond to the amide I and II band of SamS. (g) TGA analysis of ZIF-based SamS. The decomposition stage around 300 ∼ 420 °C corresponds to the decomposition of SamS. Download figure Download PowerPoint The resulting biocomposite was analyzed by a scanning electron microscope (SEM), showing a rhombic dodecahedral structure characteristic of sod-Zn(mIM)2 (Figure 1b).32,33 The sample was also analyzed by powder X-ray diffraction (PXRD), a powerful tool in characterizing MOF topology, and the result clearly revealed the sod topology of the biocomposite (Figure 1c). The catalytic activity of the resulting [email protected](mIM)2 was examined by stirring it in a solution containing ATP and l-Met, and the mixture was analyzed by high-performance liquid chromatography (HP-LC) and LC mass spectrometry (LC-MS) at different time points. This analysis showed that the expected product SAM was barely observable in the reaction, suggesting the [email protected](mIM)2 composite has no activity in SAM synthesis (Figure 2a). This result suggests that sod-Zn(mIM)2 cannot be used for immobilization of SamS. It was estimated that the aperture size of sod-Zn(mIM)2 is ∼3.4 Å, which is barely enough for 1,2,4-trimethylbenzene to diffuse in.40 Since the substrate ATP is larger than 1,2,4-trimethylbenzene, it may not be able to enter into the active site of the MOF-encapsulated enzyme for reaction. The failure in producing active SamS-ZIF composite indicated that a more general strategy needs to be established for MOF-based enzyme immobilization. Figure 2 | Enzymatic activity of homogenous (aq) SamS and ZIF-immobilized SamS. (a) Time-course analysis of SamS-catalyzed SAM production. All the enzymatic assays were carried out at the same protein concentration. (b) Relative activity of aq SamS and [email protected](mIM)2 in various harsh conditions, including 50% methanol, 75% DMSO, 50 °C, and in the presence of 0.05 mg/mL trypsin. The activities in Tris buffer were set at 100%. (c) The recyclability of [email protected](mIM)2. (d) The stability of [email protected](mIM)2 at room temperature. Download figure Download PowerPoint A recent study by Liang et al.41 showed that the precursor concentration and molar ratio between Zn2+ and mIM significantly affected the topology of enzyme-ZIF biocomposites. Motivated by this finding, we screened a series of precursor concentrations in synthesizing SamS-ZIF biocomposites, which were subsequently tested in the enzymatic assays. As shown in Table 1, biocomposite formed at high molar concentrations of mIM and Zn2+ did not show any SAM synthesis activity. The activity was gradually observed with the decreased precursor concentrations. The highest activity was observed for the sample 18 produced with the concentrations of Zn2+ and mIM at 5 and 20 mM (Table 1), and the activity was slightly lower but comparable with the enzyme in aq solution (Figure 2a). Table 1 | Relative Activities of SamS-MOF Composites Formed in Different Precursor Concentrations. The Activity Is Calculated Relatively to That of Sample 18 ([email protected](mIM)2), Which Is Set to 100% Sample Concentrations of Precursors (mM) Molar Radio Zn2+:mIM Relative Activity (%) Zn(NO3)2 mIM 1 20 1400 1:70 0 2 40 160 1:4 0 3 40 80 1:2 0 4 40 40 1:1 0 5 20 160 1:8 1 6 20 80 1:4 11 7 20 40 1:2 0 8 10 160 1:16 2 9 10 80 1:8 11 10 10 40 1:4 55 11 10 30 1:3 4 12 10 20 1:2 4 13 7.5 40 3:16 57 14 7.5 30 1:4 61 15 7.5 20 3:8 4 16 5 40 1:8 72 17 5 30 1:6 79 18 5 20 1:4 100 19 2.5 10 1:4 No precipitate To reveal the topographic features of the active biocomposite, sample 18 was analyzed by SEM, and the result showed an aggregated lamellar, nanoflower-like structure (Figure 1d and Supporting Information Figure S1). The sample was further analyzed by PXRD, and the result showed a pattern that did not match any known ZIF topologies. However, the main peaks in the PXRD spectrum matched with the new structures of unclear topologies named U12 and U14 in the recent study (Figure 1e).41 Moreover, amorphous product was observed in the sample, which was identified as Zn(OH)(NO3)(H2O),42 and this analysis was consistent with the tiny particles in the SEM image (Figure 1d and Supporting Information Figure S1). Herein, we termed the newly produced nanoflower-like biocomposite as [email protected](mIM)2. The as-prepared [email protected](mIM)2 was also analyzed by Fourier transform infrared (FTIR) spectroscopy (Figure 1f) to examine enzyme loading. Characteristic absorption bands of SamS were observed in the ranges from ∼1640 to 1660 cm−1 and from ∼1510 to 1560 cm−1, ascribed to the amide I (mainly from C=O stretching mode) and II band (mainly from a combination between of NH bending and CN stretching modes), respectively.43 In contrast, the control sample prepared from the same precursor concentration without SamS did not give these bands, confirming the encapsulation of SamS in the biocomposite. To reveal the ratio of enzyme in the [email protected](mIM)2 biocomposite, the sample was analyzed by thermogravimetric analysis (TGA). For comparative analysis, parallel TGA analysis was also performed for [email protected](mIM)2. This analysis showed that for [email protected](mIM)2, the first decomposition stage was observed between 120 and 190 °C. Approximately 18% weight loss was observed in this stage (Figure 1g), which corresponded to the loss of guest molecules such as H2O and small organic molecules.42 The next decomposition stage started from 300 °C and ended around 420 °C, which accounts for ∼4% weight loss and corresponds to enzyme decomposition. In contrast, the TGA data of [email protected](mIM)2 showed a much lower proportion (∼8 wt %) of guest molecules but a remarkably higher proportion (∼20 wt %) of immobilized enzyme (Figure 1g). The enzyme ratios were also analyzed by quantification of the enzyme remaining in the supernatant after enzyme-MOF production (see Supporting Information), and the result was consistent with those observed in TGA analysis. These results clearly suggest that the lamellar topology has a much higher efficiency in enzyme immobilization than the canonic sod topology. Nitrogen adsorption isotherm analysis was also performed for [email protected](mIM)2 and [email protected](mIM)2 to examine the porosity of MOF composites ( Supporting Information Figure S2). The results showed that [email protected](mIM)2 had a surface area of 1582 m2 g−1, and this is consistent with the TGA analysis showing that the [email protected](mIM)2 contains a large fraction of guest molecules. In contrast, the surface area of [email protected](mIM)2 was estimated to be 18.6 m2 g−1, which is more than 80-fold less than that of [email protected](mIM)2 ( Supporting Information Figure S2). These results suggest that the lamellar topology of nf-Zn(mIM)2 is nonporous, and the substrates did not access the enzyme active site through the pore network of biocomposite, but likely through the petals of the nanoflower. One of the most promising features of enzyme-MOF biocomposites is their stability and recyclability. To test whether the lamellar topology of ZIF can protect enzymes from inactivation in unfavorable conditions, [email protected](mIM)2 was treated with a series of harsh conditions, including organic solvent, high temperature, and trypsin digestion. The results showed that the biocomposite retained most of its catalytic activity in these harsh conditions. Remarkably, the biocomposite retained more than 85% activity in 75% dimethyl sulfoxide (DMSO) solvent and at 50 °C; in these conditions the enzyme in solution was completely inactivated (Figure 2b). The recyclability was analyzed by examining the activity in five consecutive cycles, in which the enzyme-MOF composite was collected from an assay mixture by centrifugation, washed three times by assay buffer, and utilized for the next round of reaction. The results showed no observable decrease in activity after five cycles (Figure 2c). Moreover, we did not see any apparent activity loss when the biocomposite was kept at room temperature (∼25 °C) for 6 weeks (Figure 2d). Together, these analyses indicate the excellent operational stability and recyclability of the lamellar SamS-MOF biocomposite produced in this study. We next selected alcohol dehydrogenase (AclDH) and tested its catalytic activity in the enzyme-MOF composite. AclDH catalyzes the interconversion of ethanol and acetaldehyde with NAD+/NADH. An early report showed that active [email protected](mIM)2 biocomposite could be synthesized by coprecipitation of AclDH with a specialized NAD+-tethered polymer, which contains phenylboronic acid ligands that link NAD+.39 In this study, we synthesized [email protected](mIM)2, which was validated by SEM (Figure 3a), PXRD ( Supporting Information Figure S3), and TGA ( Supporting Information Figure S4), all of which confirmed successful incorporation of AlcDH into the correct sod-Zn(mIM)2. To test the activity of AlcDH @sod-Zn(mIM)2, we performed a time-dependent reaction with ethanal and NAD+ in the presence of methylene blue (MB+). The latter compound is an optical reporter that can be reduced by NADH to the colorless form. No reaction was observed in the assay (Figure 3b), suggesting that [email protected](mIM)2 was not catalytically active. The reaction mixture was further examined by LC-HRMS analysis, and production of NADH was barely observed. These analyses suggest that [email protected](mIM)2 is not catalytically active, likely because NAD+ cannot enter into the active site through the small aperture of sod-Zn(mIM)2. Figure 3 | ZIF-based immobilization of AlcDH. (a) SEM analysis of [email protected](mIM)2. (b) Time-course analysis of AclDH-catalyzed MB+ reduction by ethanol. All the enzymatic assays were carried out at a similar protein concentration. (c) SEM analysis of [email protected](mIM)2. (d) Relative activity of native (aq) AclDH and [email protected](mIM)2 in various harsh conditions, including 50% methanol, 75% DMSO, 50 °C, and in the presence of 0.05 mg/mL trypsin. The activities in Tris buffer were set at 100%. Download figure Download PowerPoint We then followed a procedure similar to that for [email protected](mIM)2 and synthesized [email protected](mIM)2,39 which was characterized by SEM (Figure 3c), PXRD ( Supporting Information Figure S5), TGA ( Supporting Information Figure S4), and FTIR ( Supporting Information Figure S6), and all of these results were similar to those of [email protected](mIM)2. Subsequent analysis showed that [email protected](mIM)2 has excellent catalytic activity, which is even significantly higher than the homogeneous AlcDH in the solution (Figure 3b). This observation demonstrates the great potential of nf-Zn(mIM)2 in enzyme immobilization. The activity of [email protected](mIM)2 was also analyzed against various harsh conditions. [email protected](mIM)2 appeared to be less stable compared with [email protected](mIM)2, but still retained more than 50% of activity in 75% DMSO and at 50 °C; in these conditions the enzyme in solution was completely inactivated (Figure 3d). The biocomposite retained >75% activity after five cycles ( Supporting Information Figure S7a) and no apparent activity loss when the biocomposite was kept at room temperature (∼25 °C) for 3 weeks ( Supporting Information Figure S7b), again indicating the operational stability of the [email protected](mIM)2 biocomposite produced in this study. To further extend the application of nf-Zn(mIM)2 for enzyme immobilization, we selected the thioesterase (TE) involved in teixobactin biosynthesis.44,45 Teixobactin is a cyclic peptide antibiotic that exhibits potent activity against various drug-resistant bacteria. More importantly, no teixobactin-resistant bacterial strains were isolated despite extensive efforts, reflecting its great promise to fight against antimicrobial resistance.46 Recently, we showed that the tandem TE domain (TE1-TE2) of the Txo2 protein catalyzes the cyclization of various hendecapeptide substrates to produce teixobactin analogues (Figure 4a).44 To test whether the lamellar [email protected] biocomposite works for these large peptide substrates, we synthesized [email protected](mIM)2 by a procedure similar to that described above, and the correct topology of the resulting biocomposite was confirmed by SEM analysis (Figure 4b). Remarkably, [email protected](mIM)2 was fully active in synthesizing cyclized peptide, showing a similar catalytic efficiency with the enzyme in aq solution ( Supporting Information Figure S8). In contrast, no activity was observed for [email protected](mIM)2 ( Supporting Information Figure S8). As expected, [email protected](mIM)2 was stable, retaining >80% activity in 75% DMSO and >90% activity at 50 °C ( Supporting Information Figure S9). Figure 4 | ZIF-based immobilization of TE1-TE2. (a) TE-catalyzed synthesis of a teixobactin analog. (b) SEM analysis of [email protected](mIM)2. Download figure Download PowerPoint Conclusion We have demonstrated that, owing to the small aperture size, the traditional sod morphology of ZIF is not suitable for immobilization of enzymes that act on large substrates. Instead, we showed that the lamellar nanoflower-like ZIF produced with low precursor concentrations overcomes the aperture size limitation of sod-Zn(mIM)2 and can serve as a general carrier for enzyme immobilization. Using nf-Zn(mIM)2, various active [email protected] biocomposites were produced, including the thioesterse-based composite that acts on a peptide substrate containing 11 amino acids. These results demonstrate the remarkable tolerance of substrate size in the ZIF-immobilized enzymes. Enzyme immobilization on nf-Zn(mIM)2 also significantly increased stability and recyclability. In contrast to sod-Zn(mIM)2, the lamellar nf-Zn(mIM)2 is nonporous, and has a much higher efficiency for enzyme immobilization. The lamellar nanoflower-like ZIF framework identified in this study complements the wide interest in nanoflower structure in multiple applications such as biomedicine,47–49 and we expect it to be used extensively as a general carrier for enzyme immobilization. Supporting Information Supporting Information is available and includes the procedures for enzyme expression and purification, the protocol for the synthesis and characterization of enzyme-MOF composites, and the protocol for enzyme activity evaluation. Conflict of Interest There is no conflict of interest to report. 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