Biomimetic 1-Aminocyclopropane-1-Carboxylic Acid Oxidase

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Biomimetic 1-Aminocyclopropane-1-Carboxylic Acid Oxidase Ethylene Production by MIL-100(Fe) Based Materials Marzena Fandzloch, Carmen R Maldonado, Jorge A.R. Navarro, and Elisa Barea ACS Appl. Mater. Interfaces, Just Accepted Manuscript • DOI: 10.1021/acsami.9b13361 • Publication Date (Web): 30 Aug 2019 Downloaded from pubs.acs.org on August 30, 2019

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ACS Applied Materials & Interfaces

Biomimetic

1-Aminocyclopropane-1-Carboxylic

Acid Oxidase Ethylene Production by MIL-100(Fe) Based Materials Marzena Fandzloch,† Carmen R. Maldonado,* Jorge A. R. Navarro,* Elisa Barea* Departamento de Química Inorgánica, Universidad de Granada, Av. Fuentenueva S/N, 18071 Granada, Spain.

KEYWORDS. Metal organic framework, hydroxyapatite, hybrid material, catalysis, agriculture.

ABSTRACT. A novel core@shell hybrid material based on biocompatible hydroxyapatite nanoparticles (HA) and the well-known MIL-100(Fe) (Fe3O(H2O)2F(BTC)2·nH2O, BTC: 1,3,5benzenetricarboxylate) has been prepared following a layer-by-layer strategy. The core@shell nature of the studied system has been confirmed by IR, XRPD, N2 adsorption, TEM imaging and EDS analyses revealing the homogeneous deposition of MIL-100(Fe) on HA, leading to HA@MIL-100(Fe) rod-shaped nanoparticles with a 7 nm shell-thickness. Moreover, both MIL100(Fe) and HA@MIL-100(Fe) have demonstrated to act as efficient heterogeneous catalysts towards the biomimetic oxidation of 1-aminocyclopropane-1-carboxylic acid (ACC) into ethylene gas, a stimulator that regulates fruit ripening. Indeed, the hybrid material maintains the catalytic properties of pristine MIL-100(Fe) reaching 40% of conversion after only 20 minutes. Finally, the chemical stability of the catalyst in water has also been monitored during 21 days by ICP-MS confirming that only ca. 3% of Ca is leached.

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INTRODUCTION Ethylene is a phytohormone with a relevant role during different stages of plant growth and development, such as flowering, fruit maturation and senescence.1 Indeed, the use of ethylene has high economic impact in agriculture as this gas can be used to regulate the production cycle of some crops whose flowering and fruiting is irregular (i.e. mango and pineapple). In addition, the so-called climacteric fruits (banana, mango, avocado, etc.) are currently artificially ripen in ethylene chambers. Nevertheless, this gas involves several inconveniences due to its difficult handling, making the use of ethylene precursors desirable. For example, in plants, the conversion of the precursor 1-aminocyclopropane-1-carboxylic acid (ACC) to ethylene is catalyzed by ACC-oxidase (ACCO) protein in the presence of oxygen, ascorbic acid, Fe(II) and hydrogen carbonate.2 Noteworthy, it has been already demonstrated that some Fe(II) or Fe(III) complexes can also catalyze the degradation of ACC to ethylene gas, mimicking the enzymatic activity of ACCO.3–9 However, ethylene production from these iron complexes has been investigated mainly in organic solvents, which limits the practical application of the above mentioned compounds. Consequently, the search for alternative biomimetic ACCO like systems is of high interest. Metal-organic frameworks (MOFs) are versatile inorganic porous materials that have found a wide range of applications in the last two decades, such as separation and purification of gases, 10 heterogeneous catalysis11,12 and biomedical applications13 among others. However, only few studies have been devoted to agriculture purposes, in particular, related to the controlled release of phytoactive molecules that allows the development of smart crops. Thus, MOFs have been recently explored as potential carriers of pesticides,14 fertilizers15, antiripeners16 and ethylene gas.17,18 In this context, iron MOFs could be envisaged as attractive materials able to mimic


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ACCO catalytic activity. Among them, MIL-100(Fe) (Fe3O(H2O)2F(BTC)2·nH2O, BTC: 1,3,5benzenetricarboxylate), firstly prepared by Serre and col.,19 can be considered a good candidate for this application due to its high biocompatibility20 and the presence of accessible Fe(III) centers in its structure.19 On the other hand, it should be highlighted that the controllable assembly of MOFs on the surface of different materials (active carbon, graphene, mesoporous silica, metallic nanoparticles, etc.) usually enhances the properties of both components.21 In this context, hydroxyapatite (HA), a biocompatible material with chemical composition similar to bones, has been recently reported as substrate for the deposition of MIL-100(Fe). In particular, Zhu, Xiong and col. have prepared recyclable HA@MIL-100(Fe) nanofibers, for the detection of H2O2 and glucose by combining the peroxidase-like activity of MIL-100(Fe) with the flexibility, lightweight and thinness of HA paper.22 Analogously, Li and col. have designed hydroxyapatite nanowires functionalized with magnetic Fe3O4 nanoparticles and MIL-100(Fe) nanocrystals for the specific capture of phosphorylated peptides.23 Taking into account this background, in this work, we demonstrate the ability of MIL-100(Fe) and HA@MIL-100(Fe) rod-shaped nanoparticles to act as efficient heterogeneous catalysts in the conversion of ACC into ethylene thereby mimicking ACCO protein activity. Noteworthy, the hybrid material maintains the catalytic properties of free MIL-100(Fe) while improving its shaping (Scheme 1).


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Scheme 1. Preparation of HA@MIL-100(Fe) nanorods following a layer-by-layer method and ulterior evaluation of their catalytic properties towards the conversion of ACC into ethylene gas.

H2O2 NaHCO3

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HA@MIL-100(Fe)@ACC

EXPERIMENTAL SECTION Synthesis of the materials. All chemicals were commercially available and used without further purification. Calcium hydroxide, phosphoric acid and Fe(NO3)3·9H2O were purchased from Alfa Aesar. Na(OOCCH3)·3H2O, 1,3,5-benzenetricarboxylic acid (H3btc), FeCl3·6H2O and sodium hydrogen carbonate were purchased from Sigma-Aldrich. Hydrogen peroxide (H2O2, 30 wt%), was purchased from Merck. Absolute ethanol was purchased from VWR Chemicals. Ultra-pure water (18.2 mΩ cm-1) was used throughout. Synthesis of MIL-100(Fe). MIL-100(Fe) was prepared by a facile low-temperature synthesis previously described by Zhang et al.24 Briefly, Fe(NO3)3·9H2O (4.04 g, 10 mmol) and H3btc (1.89 g, 9 mmol) were mixed in 6 mL of water and stirred under reflux at 95 °C for 12 h. Afterwards, the resulting precipitate was washed three times with water (3 x 350 mL) and ethanol (3 x 350 mL) at 70 °C. Each washing process took 24 h. Finally, the sample was dried at 70o C overnight.


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Synthesis of hydroxyapatite nanoparticles (HA). HA nanoparticles (Ca10(PO4)6(OH)2) with rodlike shape were synthesized according to a previous method with some modifications. 25 Typically, slow addition of H3PO4 (0.15 M) to an aqueous suspension of Ca(OH)2 (ca. 0.17 M) resulted in the precipitation of HA. The reaction mixture was then stirred at 37 °C for 24 h and left standing for other 24 h. The precipitate was washed with water (3 x 10 mL), centrifuged at 4,000 rpm and dried at 70o C overnight. In order to obtain the desired rod-like shape, the HA powder was hydrothermally treated.25 For this purpose, HA nanoparticles were suspended in water (15 mg/mL), placed in an acid digestion bomb (Parr), and heated at 200o C for 24 h. After cooling to RT, the HA powder was washed with water and dried at 70 o C overnight. In order to quantify the content of Ca and P of the hydroxyapatite by ICP-OES, 4.7 mg and 5.0 mg of HA@MIL-100(Fe) were degraded in 3.76 mL and 4 mL of concentrated HNO3 (69 %), respectively. After 48 hours, the samples were diluted 100 times by mixing 100 µL of each solution with 200 µL of concentrated HNO3 (69 %) and 9700 µL of water (final HNO3 concentration = 2%). ICP-OES: Ca/P ratio = 1.79. Synthesis of [Fe3O(OOCCH3)6OH]·2H2O cluster. [Fe3O(OOCCH3)6OH]·2H2O was synthesized according to a previously published method.26 Typically, Fe(NO3)3·9H2O (8.00 g, 20 mmol) and Na(OOCCH3)·3H2O (11.00 g, 81 mmol) were dissolved in water (9 mL) and stirred under RT overnight. The resulting precipitate was filtered, washed with cold water (1 x 20 mL) and dried at 100°C. Anal. Calc. for [Fe3O(OOCCH3)6OH]·2H2O: C, 24.39; H, 3.92. Found: C, 23.68; H, 3.96. Synthesis of HA@MIL-100(Fe) nanorods. The HA@MIL-100(Fe) core-shell nanoparticles were prepared following a modification of the layer-by-layer method reported by Zhu, Xiong and col.22 In particular, 200 mg of HA were suspended in an ethanolic solution of 1,3,5-


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benzenetricarboxylic acid (10 mL, 10 mM) and the mixture was stirred at 60oC for 30 min. Afterwards, the solid was centrifuged (4,000 g / 30 min) and washed with ethanol (1 x 10 mL). The resulting material was then soaked in an ethanolic solution of [Fe3O(OOCCH3)6OH]·2H2O cluster (10 mL, 10 mM) at 60oC for 15 min. Similarly, the resulting product was centrifuged and washed with ethanol (1 x 10 mL). This procedure, which constitutes one cycle of the layer by layer process, was repeated 10 times. Finally, HA@MIL-100(Fe) hybrid material was dried at 70o C overnight. In order to quantify the content in Fe, Ca and P of the hybrid material by ICPOES, 1.6 mg and 1.2 mg of HA@MIL-100(Fe) were degraded in 406 µL and 305 L of concentrated HNO3 (69 %), respectively. After 48 hours, the samples were diluted 100 times by mixing 100 µL of each solution with 200 µL of concentrated HNO3 (69 %) and 9700 µL of water (final HNO3 concentration = 2%). Based on ICP-OES and TG data the formula 1 mol [email protected] mol MIL-100(Fe) was proposed. ICP-OES: Ca/Fe = 2.35, P/Fe = 1.43, Ca/P = 1.65. TGA residue (Ca10(PO4)6(OH)[email protected] mol 3/2Fe2O3) (calc./exp.): 70/67%. Catalytic tests: ethylene production Experiments in the presence of hybrid material. The hybrid (19.1 mg) was placed in a 65 mL septum-equipped flask and, after degassing in vacuum, degassed solutions of ACC (5 mg dissolved in 1.5 mL of water), sodium hydrogen carbonate (50 mM, 1 mL) and hydrogen peroxide (30%, 5 L) were injected through the septum. Ethylene production was monitored up to 3 hours at room temperature by injecting 30 µL of the headspace gas with a gastight syringe into a gas chromatograph. These experimental conditions correspond to a 1:5:5 molar ratio of hybrid:ACC:H2O2. In the case of 1:10:10 molar ratio, 9.7 mg of ACC and 10 L of hydrogen


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peroxide were used. Similarly, 19.5 mg of ACC and 20 L of H2O2 were assayed for the 1:20:20 molar ratio and 100 mg of ACC and 102 L of H2O2 were tested for the 1:100:100 molar ratio. Control experiment in the presence of HA. HA (10.0 mg) was placed in a 65 mL septumequipped flask and, after degassing in vacuum, degassed solutions of ACC (5 mg dissolved in 1.5 mL of water), sodium hydrogen carbonate (50 mM, 1 mL) and hydrogen peroxide (30%, 5 L) were injected through the septum. Ethylene production was monitored up to 3 hours at room temperature by injecting 30 µL of the headspace gas with a gastight syringe into a gas chromatograph. These experimental conditions correspond to a 1:5:5 molar ratio of HA:ACC:H2O2. Control experiment in the presence of MIL-100(Fe). MIL-100(Fe) (9.1 mg) was placed in a 65 mL septum-equipped flask and, after degassing in vacuum, degassed solutions of ACC (5 mg dissolved in 1.5 mL of water), sodium hydrogen carbonate (50 mM, 1 mL) and hydrogen peroxide (30%, 5 L) were injected through the septum. Ethylene production was monitored up to 3 hours at room temperature by injecting 30 µL of the headspace gas with a gastight syringe into a gas chromatograph. These experimental conditions correspond to a 1:5:5 molar ratio of MIL-100(Fe):ACC:H2O2. Catalyst recyclability assays of the HA@MIL-100(Fe) nanorods. The recyclability of HA@MIL100(Fe) was explored by analyzing ACC conversion up to four consecutive cycles for the 1:5:5 molar ratio. For this purpose, HA@MIL-100(Fe) was recovered after one catalytic cycle, washed with 10 mL of water and dried at 70 oC. The recycled hybrid was again introduced into a freshly prepared mixture (ACC: 5 mg dissolved in 1.5 mL of water, sodium hydrogen carbonate: 50


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mM, 1 mL and hydrogen peroxide: 30%, 5 L) and ethylene production was monitored. After each cycle, the recovered hybrid material was characterized by XRPD and XPS. Aqueous stability tests. 1 mL water suspensions of MIL-100(Fe) (7.2 mg/mL) and HA@MIL100(Fe) (15 mg/mL) were stirred at room temperature for 1, 3, 6, 12, 24, 48 and 72 hours and 1, 2, 3 and 4 weeks. At each time, the samples were centrifuged (20,000 g / 20 min) and the supernatants were collected. Afterwards, each solution was diluted 20 times by mixing 500 µL of the supernatant with 300 µL of concentrated HNO3 (69 %) and 9200 µL of water. The concentration of Ca, P and Fe were determined by ICP-MS. ACC Adsorbate location by computational modelling. Computational modelling of the interaction of ACC molecules with MIL-100(Fe) host framework was carried with the BIOVIA Materials Studio 2018 (Dassault Systèmes BIOVIA, Materials Studio, 2018, San Diego: Dassault Systèmes, 2018) Adsorption Locator module in order to identify the possible adsorption configurations of the studied substrates in the MOF pores by carrying out Monte Carlo searches of the configurational space of the substrate-adsorbate system. Other equipment. All solid products were analyzed by XRD using a X'Pert PRO diffractometer (PANalytical) (Department of Mineralogy, University of Granada) with the following instrumental parameters: Cu Kα-radiation (λ=1.5405 Å), current=40 mA, tension=45 kV, measurement range=3–50°2θ, time per step=4 s, and step size=0.04°2θ. To minimize orientation effects, powder samples were back loaded into the sample holders and diffraction patterns were collected under constant sample rotation. For the catalytic recyclability tests, XRPD data were collected on a Bruker D2-PHASE diffractometer (2) using CuKα radiation (λ = 1.5418 Å) and LYNXEYE detector (Department of Inorganic Chemistry, University of Granada) by scanning in


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the 5-60° 2θ range with 1.00° step. Thermogravimetric analysis were performed using a Shimadzu TGA-50H at a heating rate of 10oC min-1 in flowing air (CIC, University of Granada). N2 adsorption isotherms were measured at 77 K on a Micromeritics 3Flex Surface Characterization Analyzer. Prior to isotherm acquisition, the materials were activated and outgassed (120 ºC, 10-1 Pa) for 6 hours (Department of Inorganic Chemistry, University of Granada). Infrared spectra were collected in a Fourier transform infrared spectrophotometer (FTIR) Bruker Tensor 27, using KBr as dispersing agent (Department of Inorganic Chemistry, University of Granada). Elemental (C, H, N, S) analyses were obtained by Vario EL Cube CHNS elemental analyzer (Elementar Analysensysteme GmbH) (Faculty of Chemistry, University of Wrocław). Inductively Coupled Plasma Mass Spectrometry analysis (ICP-MS) was carried out in a NexION 300D (Perkin Elmer) while Inductively Coupled Plasma Optical Emission Spectrometry analysis (ICP-OES) was carried out in an Optima 7300DV (Perkin Elmer) (SCAI, University of Málaga). TEM images and Energy Dispersive X-ray (EDX) elemental mapping were performed using a FEI Talos F200X microscope (SCAI, University of Málaga). Samples were prepared by dispersing a small amount of the material (~3 mg) in absolute ethanol (1 mL) followed by sonication for 10 min and deposition on a copper grid. XPS measurements were recorded in a X-ray photoelectron spectrometer Kratos Axis Ultra-DLD (CIC, University of Granada). Catalytic studies were performed in Varian 450-GC Gas Chromatograph (Department of Inorganic Chemistry, University of Granada) equipped with an Agilent 30 m-column (0.53 mm internal diameter). The following conditions were used: vector = N2, Tinjector = 250°C, Toven = 150°C, Tdetector = 300°C. Ethylene was quantified from the calibration curve.


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RESULTS AND DISCUSSION The preparation of MIL-100(Fe) was carried out, under HF-free conditions, according to a previously reported low-temperature method (for more details see Supporting Information).24 The synthesized MIL-100(Fe) was systematically characterized by XRPD, N2 adsorption, TGA and IR, confirming the purity of the isolated material (see Supporting Information). Besides, TEM analysis showed agglomerated particles bigger than 200 nm (Figure S1). On the other hand, hydroxyapatite nanoparticles, Ca10(PO4)6(OH)2, were precipitated by slow addition of phosphoric acid into a calcium hydroxide solution.25 Afterwards, a post-synthetic hydrothermal treatment27 was applied in order to reduce HA agglomeration and improve particle morphology. Indeed, this treatment smoothed significantly HA surface contour, giving rise to well defined rod-shaped particles (68 ± 22 nm long and 27 ± 5 nm wide) (Figure S2). In addition, ICP-OES studies were performed revealing that experimental Ca/P ratio well matches the theoretical value (1.79 vs. 1.67, respectively). Regarding the hybrid material HA@MIL-100(Fe), it was synthetized following a modification of the layer-by-layer protocol described by Zhu, Xiong and col.22 Briefly, thermally treated HA nanoparticles were suspended in an ethanolic solution, containing H3BTC ligand, and kept at 60ºC during 30 minutes. Afterwards, the nanoparticles were recovered by centrifugation, washed with fresh ethanol and resuspended, at 60ºC for 15 minutes, in an ethanolic solution of [Fe3O(OOCCH3)6OH] cluster, previously prepared according to literature.26 The resulting core@shell nanoparticles were washed and centrifuged prior to the following cycle. This process was repeated 10 times.


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Once the hybrid material was isolated, the deposition of MIL-100(Fe) onto HA nanoparticles surface was firstly confirmed by IR spectroscopy. Indeed, the characteristic bands of both HA (1092-1046 cm-1) and BTC ligand (1618-1377 cm-1 region attributed to C=O and C=C stretching vibrations and two peaks at 764 and 714 cm−1 associated to C–H bending vibrations)22 appeared in the hybrid material (Figure 1). Additionally, XRPD studies also confirmed the dual nature of the hybrid material as a broad signal in the same region of the most intense reflections of MIL100(Fe) (3-7º range) as well as the characteristic HA diffraction peaks were observed in HA@MIL-100(Fe) pattern (Figure S3). TEM images demonstrated that HA@MIL-100(Fe) maintains the same rod-shaped morphology than hydrothermally treated HA nanoparticles with an additional shell thickness of ca. 7 nm (Figure 2). In order to further confirm the core@shell nature of the hybrid material, EDS elemental mapping was recorded. In fact, while Ca and P signals were detected mainly in nanoparticles core, Fe was preferentially localized on nanoparticles surface (Figure 2). In addition, this MOF coating increased significantly the BET surface area from 45 m2 g-1, for hydrothermally treated HA nanoparticles, to 190 m2 g-1 for HA@MIL-100(Fe) (Figure S4). On the other hand, XPS also confirmed the presence of Ca and P due to HA core, with binding energies of 349.2 and 345.8 eV for Ca 2p 1/2 and 2p3/2, respectively, and 132.0 eV for P 2p. Besides, two main peaks centered at 723.5 and 709.9 eV and their respective satellites (715.3 and 730.7 eV) were assigned to the presence of Fe3+ from MIL100(Fe) (Figure S5). Finally, the chemical composition of the hybrid material was calculated as 1 mol [email protected] mol MIL-100(Fe) based on ICP-OES and TGA studies (see Supporting Information, Figure S6).


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Figure 1. IR spectra of HA (blue), HA@MIL-100(Fe) (red), MIL-100(Fe) (green). IR spectrum of the hybrid material shows the characteristic bands of both HA and MIL-100(Fe).

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Figure 2. TEM images of a) pristine HA, b) hydrothermally treated HA nanoparticles and c) HA@MIL-100(Fe). d) EDS elemental mapping of the hybrid material demonstrating the presence of calcium and phosphorous in the core and iron in the shell.

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Once the materials were fully characterized, we have studied the potential catalytic activity of MIL-100(Fe) and HA@MIL-100(Fe) towards the oxidative conversion of ACC into ethylene gas. As far as we know, this is the first report on ethylene production from ACC precursor using a metal-organic framework as catalyst. In the first place, we evaluated the accessibility of ACC molecules to the pore voids of MIL-100(Fe) by means of Monte Carlo searches of the configurational space of the substrate-adsorbate system using BIOVIA Materials Studio 2018 Adsorption Locator module. The results showed that ACC substrate is able to diffuse through MIL-100(Fe) pore structure with preferential accommodation in the pentagonal windows and close contact to the Fe3O SBUs (Figure S7). After this initial computational assessment, we proceeded with the study of ethylene generation from degassed aqueous solutions of ACC in the presence of hydrogen peroxide, hydrogen carbonate and pristine MIL-100(Fe) or HA-supported MIL-100(Fe) (see details in Supporting Information). The kinetic profile of ethylene was monitored by gas chromatography during 3 hours at room temperature revealing that both pristine MIL-100(Fe) and HA@MIL-100(Fe) material act as efficient catalysts (Figure 3). In particular, for a 1:5:5 molar ratio (hybrid:ACC:H2O2), a 40% of conversion was reached after only 20 minutes which, taking into account the proposed formula for the hybrid (see above), corresponds to the generation of 1.4 mol ethylene per mol MIL-100(Fe). Likewise, an equimolecular amount of free MIL-100(Fe) exhibited a similar kinetic profile and ethylene production than the hybrid material (37% of conversion after 20 minutes). In contrast, HA nanoparticles did not show any ACC conversion and only a 2% of conversion was achieved in the absence of catalyst in the same timeframe.


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Figure 3. a) Proposed mechanism for ethylene production using MIL-100(Fe) catalytic active sites. b) ACC conversion into ethylene gas in the presence of HA, MIL-100(Fe) or HA@MIL100(Fe). The dotted black line indicates the effect of removal of the hybrid material by filtration to demonstrate the heterogeneity of the catalytic process. Experimental details for HA@MIL100(Fe) catalytic test: 20 mM NaHCO3, 1:5:5 molar ratio (hybrid:ACC:H2O2). The quantity of MIL-100(Fe) used for this study was normalized according to hybrid composition.

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Taking into account these promising results, we decided to further investigate the catalytic properties of the hybrid system. Firstly, and in order to demonstrate that this material behaves as a heterogeneous catalyst, HA@MIL-100(Fe) was removed from the mother solution by filtration revealing that no additional conversion of ACC into ethylene occurred (Figure 3). Noteworthy, to the best of our knowledge, this is the first example in which a heterogeneous catalyst is used to produce ethylene from ACC. Indeed, all the previously reported studies have been focused on the use of iron3–9 and copper28,29 complexes as homogeneous catalysts. Moreover, other hybrid:ACC:H2O2 molar ratios (1:10:10, 1:20:20 and 1:100:100) were also tested with the aim of confirming if smaller amounts of HA@MIL-100(Fe) could efficiently degrade ACC into ethylene gas. In all cases, similar ACC conversion profiles were obtained resulting, respectively, in 2.2, 4.6 and 8.6 mol of ethylene per mol of catalyst (MIL-100(Fe)) after 180 minutes of incubation (Figure 4). According to these results, when the amount of catalyst is reduced by half or a quarter, similar conversion yields are reached (32 and 34 % for 1:10:10 and 1:20:20 ratios, respectively, vs. 40% for 1:5:5 ratio). Nevertheless, it should be noted that conversion efficiency only decreased four times (12%) when twenty times less of HA@MIL-100(Fe) was employed (1:100:100 ratio), suggesting that our hybrid material behaves like a real catalyst with a turnover of ca. 10 mol of ethylene. Besides, the recyclability of HA@MIL-100(Fe) was explored for the 1:5:5 molar ratio by analyzing ACC conversion up to four consecutive cycles (Figure S8). Ethylene production decreased significantly after each use generating 1.4, 0.9, 0.3 and 0.2 mol of ethylene per mol of MIL-100(Fe) after the first, second, third and fourth cycle, respectively. Additionally, the catalyst was recovered and analyzed by different techniques in order to check its integrity before the following cycle. On the one hand, no appreciable changes neither in XPS spectra nor in X-ray powder diffractograms were noticed (Figures S9 and S10). On the other


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hand, ICP-OES studies revealed that, under catalytic experimental conditions, iron leaching was less than 4% after the first cycle, bellow 2.5% after the second one, and negligible from the third cycle onwards. Taking into account all these results, the decrease in ethylene production after reuse of the catalyst may be attributed to a progressive poisoning of its active sites as no evident degradation of the hybrid material was observed. This poisoning may be due to the coordination of cyanide, produced as subproduct during ACC oxidation process, to the iron metal centers (Figure 3a). In order to further explore the chemical stability of the catalyst, HA@MIL-100(Fe) was also monitored in water by means of ICP-MS during 21 days. According to our analyses, P and Fe were not detected along the whole timeframe while only around 3.7% of Ca was leached after three weeks (3% of Ca after 72 h) (Figure S11). Figure 4. Ethylene production profiles in the presence of different hybrid:ACC:H2O2 molar ratios.

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CONCLUSIONS In this work, we have demonstrated that MIL-100(Fe) both in pristine form and supported on HA rod-shaped nanoparticles behaves as an efficient ACCO biomimetic heterogeneous catalyst as a consequence of the facile diffusion of ACC substrate to the catalytically active Fe 3O SBUs. Noteworthy, the deposition of the iron MOF, onto the surface of HA, does not reduce its catalytic activity, which is of interest for practical application on other supports such as monoliths.

ASSOCIATED CONTENT Supporting Information. The Supporting Information is available free of charge on the ACS Publications website. A PDF file including TEM images, X-ray powder diffractograms, N2 adsorption isotherms, XPS data, TG analysis, and ICP-MS is provided. AUTHOR INFORMATION Corresponding Authors Carmen R. Maldonado: [email protected] Jorge A. R. Navarro: [email protected] Elisa Barea: [email protected] Present Addresses † Faculty of Chemistry, University of Wrocław, F. Joliot-Curie 14, 50-383 Wrocław, Poland.


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ORCID: Marzena Fandzloch: 0000-0001-9231-6915 Carmen R. Maldonado: 0000-0002-4958-6052 Jorge A. R. Navarro: 0000-0002-8359-0397 Elisa Barea: 0000-0001-9895-1047 Author Contributions The manuscript was written through contributions of all authors. All authors have given approval to the final version of the manuscript. ACKNOWLEDGMENT The Spanish Ministry of Economy and Competitivity and UE Feder Program (project CTQ201784692-R), University of Granada (MF, Programa de Estancias de Investigadores Extranjeros en Departamentos e Institutos) and University of Granada-Junta de Andalucía (Operative Program Feder Andalucía 2014-2020, project: B-FQM-364-UGR18), are gratefully acknowledged for generous funding. This study was partially supported by the “Unidad de Excelencia de Química Aplicada a Biomedicina y Medioambiente” (University of Granada).


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TOC

H2O2 NaHCO3 catalysis

HA@MIL-100(Fe)

HA@MIL-100(Fe)@ACC


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Biomimetic 1-Aminocyclopropane-1-Carboxylic Acid Oxidase

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