Postmetalated Zirconium Metal Organic Frameworks as a Highly

Article pubs.acs.org/IC

Postmetalated Zirconium Metal Organic Frameworks as a Highly Potent Bactericide Boushra Mortada, Tamara Abou Matar, Aya Sakaya, Hala Atallah, Zeinab Kara Ali, Pierre Karam,* and Mohamad Hmadeh* Chemistry Department, American University of Beirut, P.O.Box 11-0236, Riad El-Solh, 1107 2020 Beirut, Lebanon S Supporting Information *

ABSTRACT: Metal−organic frameworks (MOFs) have emerged as an important class of hybrid organic−inorganic materials. One of the reasons they have gained remarkable attention is attributed to the possibility of altering them by postsynthetic modification, thereby providing access to new and novel advanced materials. MOFs have been applied in catalysis, gas storage, gas separation, chemical sensing, and drug delivery. However, their bactericidal use has rarely been explored. Herein, we developed a two-step process for the synthesis of zirconium-based MOFs metalated with silver cations as a potent antibacterial agent. The obtained products were thoroughly characterized by powder X-ray diffraction, scanning electron microscopy, UV− visible, IR, thermogravimetric, and Brunauer−Emmett−Teller analyses. Their potency was evaluated against E. coli with a reported minimal inhibitory concentration and minimal bactericidal concentration of as low as 6.5 μg/mL of silver content. Besides the novelty of the system, the advantage of this strategy is that the MOFs could be potentially regenerated and remetalated after each antibacterial test, unlike previously reported frameworks, which involved the destruction of the framework.

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INTRODUCTION

or S (thiols) donors of biological ligands (e.g., nucleic acids, proteins, cell membranes).9 Metal−organic frameworks (MOFs) constitute a family of hybrid inorganic−organic solid materials that are known for being highly porous and crystalline.10−13 They are formed by the self-assembly of metal cations with polytopic organic ligands. Their high versatility, which is attributed to the wide range of starting materials (metal ions and organic ligands) from which they can be synthesized, has led to their application in different fields. These include gas separation, gas storage, catalysis, and sensing.14−16 As an approach toward applying MOFs as antibacterial agents, few silver-based MOFs have been recently synthesized and studied. Characterized by their high effectiveness against a wide range of bacteria, long-term persistence, in addition to the thermal and optical stabilities, these silver-based MOFs are considered to be the “third-wave” of antibactericide with potency greater than many other silver salts or silver-containing complexes previously studied.8,17 Examples include the synthesis of MOFs [Ag2(O-IPA)(H2O)· (H3O)] and [Ag5(PYDC)2(OH)], under hydrothermal conditions, using aromatic−carboxylic acids containing hydroxyl and pyridyl groups as ligands. Both compounds exhibited

The increasing resistance of microorganisms to traditional antibiotics has spurred, in recent years, an intensive research effort to find new antimicrobial agents.1−3 Transition metals have gained increasing attention as new bactericidal agents.4−6 Cobalt-based MOFs were shown to be highly potent with a reported minimal bactericidal concentration (MBC) of 15 ppm.7 Silver-containing compounds are known for being effective against a wide range of bacteria, including Grampositive and Gram-negative strains. This has caused both inorganic silver salts and hybrid organic−inorganic materials containing silver (mainly silver complexes) to be increasingly utilized in numerous consumer products and medical devices, including cosmetics, ceramics, surgical devices, and wound dressings. It is believed that the release of Ag+ ions from silverbased materials into the surrounding environment is the key to their antibacterial activity.8 However, the exact mechanism by which the silver ions inhibit the microorganism growth is still elusive. Nonetheless, minimum inhibitory concentration (MICs) experiments have shown broader antimicrobial activity spectra for silver complexes with Ag−O and Ag−N bonds than for those with Ag−P and Ag−S bonds. This is due to the weak nature of the Ag−O and Ag−N bonds, where Ag−O bonding complexes can readily undergo ligand replacement with O, N, © 2017 American Chemical Society

Received: February 16, 2017 Published: March 24, 2017 4739

DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744

Article

Inorganic Chemistry

Scheme 1. Synthesis of UiO-67-bpydc and Its Metalated Form UiO-67-bpydc-Ag (a) and UiO-66-2COOH and Its Metalated Form UiO-66-2COOAg (b)

Figure 1. (a) PXRD pattern of simulated UiO-67-bpydc (black), activated UiO-67-bpydc (blue), UiO-67-bpydc-Ag (red), simulated UiO-66− 2COOH (green), activated UiO-66−2COOH (gold), and UiO-66−2COO-Ag (purple). (b) SEM images of UiO-67-bpydc (A), UiO-67-bpydc-Ag (B), UiO-66−2COOH (C), and UiO-66−2COOAg (D).

and the metal node, respectively, in addition to postmetalation.20−22 Because of the strong chemical bonding and higher coordination number, the Zr-based secondary-building unit (SBU) Zr6O4(OH)4(CO2)12, found in UiO-66 (Zr6O4(OH)4(BDC)6 BDC = terephthalate), is one of most stable inorganic clusters.23 Thus, this inorganic SBU appears as a notable platform for the construction of thermally and chemically stable MOFs. Herein, we present a new strategy for the synthesis of silvercontaining antibacterial agents based on MOFs, following a two-step process. In the first step, chemically stable zirconiumbased MOFs are synthesized; UiO-67-bpydc (using 2,2′bipyridine-5,5′-dicarboxylic acid as linker) and UiO-66− 2COOH (using 1, 2,4,5-benzenetetracarboxylic acid as linker).

excellent and long-term antimicrobial activities toward Gramnegative bacteria Escherichia coli and Gram-positive bacteria Staphylococcus aureus.9 Other reported silver-based MOFs were synthesized using phosphobenzoic acids, which showed high silver ion release capacities.18 Since the silver clusters employed to build these MOF structures are chemically unstable, the release of silver cations occurs via the destruction of the frameworks. The possibility of functionally altering MOFs, after their synthesis and isolation, by postsynthetic modification (PSM), leads to the formation of advanced MOF materials that are suitable for more specialized applications.14,15,19 The major PSM strategies for functionalizing MOFs include covalent and coordinate covalent modifications, applied to the organic linker 4740

DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744

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Inorganic Chemistry

Figure 2. (a) IR spectrum of bpydc linker (black), UiO-67-bpydc (blue), UiO-67-bpydc-Ag (red), 1,2,4,5-benzene tetracarboxylic acid (green), UiO66−2COOH (yellow), and UiO-66−2COOAg (purple). (b) TGA curve of UiO-67-bpydc (blue), UiO-67-bpydc-Ag (red), UiO-66−2COOH (gold), and UiO-66−2COOAg (purple). (c) UV−visible spectrum of UiO-67-bpydc (blue), UiO-67-bpydc-Ag (red), UiO-66−2COOH (gold), and UiO-66−2COOAg (purple).

vibration of the carboxylate group (COO−). This is in addition to the appearance of the peak at 670 cm−1 that corresponds to the Zr−O bond.23,26 The CN stretching vibration (1600 cm−1) in UiO-67-bpydc indicated the presence of free bipyridyl groups that will later provide an access for the silver cations during postsynthetic modification. The IR spectrum of the UiO-66−2COOH indicated the presence of two new bands at 750 and 1413 cm−1 that correspond to the Zr−O and carboxylate group (COO−) symmetric stretching vibrations, respectively. However, the retention of the free CO at 1700 cm−1 and O−H stretching vibrations at 2500−3100 cm−1 in UiO-66−2COOH proved the existence of free noncoordinating carboxyl groups in the framework. To assess the porosity of the MOF structures, N2 adsorption/desorption isotherms (77 K) of the activated samples were measured, and the Brunauer− Emmett−Teller (BET) surface areas were determined to be 2024 and 270 m2·g−1 for UiO-67-bpydc and UiO-66−2COOH, respectively. These values are in good agreement with the previously reported values for the same structures (Figures S3 and S6). The lower porosity exhibited by UiO-66−2COOH, as compared with that of UiO-66 MOFs reported in the literature (BET surface area of UiO-66 synthesized from 1,4 benzenedicarboxylic acid = 850 m2·g−1), was ascribed to the steric hindrance caused by the free carboxyl groups of the linker.23,27 To determine the thermal stability of the two structures, thermogravimetric analysis was performed and showed that UiO-67-bpydc was thermally stable up to 430 °C, whereas UiO-66−2COOH was stable up to 350 °C. Above this temperature the weight loss observed can be attributed to the degradation of the organic network, leading to the formation of ZrO2 (Figure 2b). After the synthesis and characterization of UiO-67-bpydc and UiO-66−2COOH, the two compounds were postmetalated with silver cations at the exposed binding units (bpy chelating groups and carboxylate units in UiO-67-bpydc and UiO-66− 2COOH, respectively). To this end, MeOH solutions containing a 1:2 mass ratio of the Zr-MOFs and AgNO3 were heated at 50 °C for 20 h, yielding a yellow-brownish microcrystalline powder (Scheme 1). The obtained materials were then extensively washed with methanol to remove the physically adsorbed silver cations, and the colors of both powders were retained even after washing several times, thus indicating that silver cations were inserted in the bipyridyl units

The free noncoordinating pyridyl and dicarboxyl groups of the bpydc and 1,2,4,5-benzenetetracarboxylic acid organic linkers, respectively, present open metal-binding sites, such that in the second step, the synthesized MOF materials can be postmetalated with silver cations at these free coordination sites. The bactericidal activity of the obtained silver−metalated MOFs is evaluated, which revealed good potency with a calculated MIC and MBC of 6.5 μg/mL of silver content.

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RESULTS AND DISCUSSION

The Zr-based SBU Zr6O4(OH)4(CO2)12, found in this series of MOFs, is one of the most stable inorganic clusters due to the strong chemical bonding and higher coordination number.23,24 It therefore constitutes a notable platform to construct the thermally and chemically stable MOFs, which is critical for antibacterial applications. As such, two Zr-based MOFs that incorporate open binding units for postmetalation with silver were chosen, namely, the UiO-66−2COOH25 and UiO-67bpydc,8 containing free carboxylate and free bipyridyl groups, respectively (Scheme 1). Both of these were synthesized following new and facile solvothermal approaches (see Experimental Section for more details). The high crystallinity and phase purity of the samples were confirmed by powder X-ray diffraction (PXRD; Figure 1a and Figure S2). Scanning electron microscopy (SEM) revealed an octahedral morphology of the obtained compounds with a crystal size ranging from 0.1 to 2 μm for both MOF materials (Figure 1b). To ensure that the extra binding units (two carboxylate units of the 1,2,4,5-benzenetetracarboxylic acid and the bipyridyl sites of the bpydc) are not involved in the coordination during the formation of the MOF structure, IR spectroscopy was employed, and the obtained spectra were compared to those of the free linkers (Figure 2b). On one hand, IR spectrum of UiO-67-bpydc showed a broad and intense band centered at 3350 cm−1 that corresponds to physisorbed water molecules condensed in the MOF pores. On the other hand, the vibrations of the hydroxyl moiety of the free linker (2500−3000 cm−1) were no longer present in the MOF spectrum. The free CO stretching vibration of the ligand (1700 cm−1) was shifted to a lower wavenumber in the MOF spectrum. The intense doublet at 1590 that overlaps with the peak from CN stretching vibration and 1390 cm −1 corresponds to the in-phase and out-of-phase stretching 4741

DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744

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Figure 3. (a) Optical density measurement for E. coli grown in the presence of incremental concentation of UiO-66−2COOAg. The error bars represent the standard deviation of three independent measurements. The lines connecting the experimental points are for visual aid. (b) Agar plated solutions (50, 75, 100, and 200 μg/mL) to determine the minimum bactericidal concentration. The 50 μg/mL was diluted 1 × 105 prior to plating. (c) Optical density measurement for E. coli grown in the presence of incremental concertation of UiO-67-bpdc-Ag. The error bars represent the standard deviation of three independent measurements. The lines connecting the experimental points are for visual aid. (d) Agar-plated solutions (50, 75, 100, and 200 μg/mL) to determine the minimum bactericidal concentration.

a decrease in porosity upon metalation (Figure S3 and Figure S6) and the calculated BET surface areas dropped from 2024 to 700 m2 g−1 For UiO-67-bpydc and from 270 to 67 m2 g−1 for UiO-66−2COOH after metalation. The amount of silver ions incorporated into the MOF structures was evaluated using atomic absorption spectroscopy and was found to be 0.13 and 0.12 g per one gram of MOF for UiO-67-bpydc-Ag and UiO66−2COOAg, respectively. As a proof of concept, the antibacterial activity of the prepared zirconium MOFs postmetalated with silver was evaluated against E. coli. Concentrations ranging between 1 and 200 μg/mL of MOF were tested (Figure 3). Both metalated frameworks showed bactericidal activity with a calculated MIC and MBC of 50 μg/mL equivalent to 6.5 μg/ mL of silver content for UiO-67-bpdc-Ag. An MIC of 75 μg/ mL and an MBC of 100 μg/mL for UiO-66−2COOAg equivalent to 0.9 and 0.12 μg/mL of silver content were also reported. The MIC was determined by measuring the optical density at 600 nm after 3, 6, 12, and 22 h of incubation time. The difference in the inhibition was attributed to the silver release from the MOF structures. As seen in Figure S9, 0.85% of the silver was released for UiO-67-bpdc-Ag compared to 0.53% for UiO-66−2COOAg. When compared to previously reported silver-based material, the microstructures showed good potency. Two recent silverbased MOFs by Lu et al. were shown to have antibacterial activity with MIC of 5 and 10 μg/mL.28 Berchel et al. tested the antibacterial activity of Ag-based MOFs against six microorganism strains with a reported minimum inhibition concentration of 50 μM against E. coli.29 Liu et al. reported three Ag-MOF structures with a reported MIC of ca. 300 μg/ mL.30 Unlike these structures, where silver or other active

and bicarboxylates coordination sites of UiO-67-bpydc and UiO-66−2COOH, respectively. SEM and PXRD patterns of the metalated versions supported the hypothesis that the underlying frameworks were maintained after postsynthetic modification. Metalation was confirmed qualitatively through TGA, IR, BET analysis, and UV−visible spectroscopies, and the degree of silver functionalization was quantified by atomic absorption spectroscopy. The TGA traces for Ag-containing compounds showed two decomposition steps, unlike the free versions that exhibited only one major decomposition step (Figure 2b). IR spectroscopy should be very useful to characterize the metalation process. Indeed, the CN, O−H, and CO stretching vibrations of the bipyridyl and of the dicarboxylate functional groups should be affected. On one hand, IR spectrum of UiO-66−2COOAg revealed the disappearance of the O−H and free CO stretching vibrations at 2500−3100 and 1700 cm−1, respectively, thus indicating the coordination of the free carboxyl groups in the parent MOF to the silver cations. On the other hand, due to the overlap of the bands from CN and carboxylate group stretching vibrations (as it can be seen in the spectrum of UiO-67-bpydc-Ag), it is difficult to indicate the coordination of the pyridyl groups to silver cations in UiO-67-bpydc from IR spectroscopy (through the disappearance of the CN band; Figure 2a). However, the change in color, from white to yellow, observed during metalation, provides an evidence of the coordination. In this regard, UV−visible spectroscopy was employed. UV−visible spectra of the metalated compounds showed a wide band centered around 450 and 550 nm for UiO-67-bpydc-Ag and UiO-66−2COOAg, respectively (Figure 2c). Furthermore, N2 isotherms of UiO-67-bpydc-Ag and UiO-66−2COOAg indicate 4742

DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744

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Inorganic Chemistry

with MeOH. The obtained product was collected by centrifugation and dried under dynamic vacuum at 80 °C. Synthesis of UiO-67-Ag-(bpydc). In a 20 mL scintillation vial, silver nitrate (AgNO3; 40 mg) was dissolved in MeOH (10 mL) by sonication for 10 min. UIO-67-bpydc (20 mg) was then added to the silver solution. The reaction mixture was then stirred on a hot plate at 50 °C for 20 h. The resulting brownish microcrystalline powder was centrifuged, and the supernatant was discarded. The solids were washed with MeOH for 2 d, and the solution was exchanged with fresh MeOH two times per day. The solids were collected by centrifugation and dried under dynamic vacuum at 110 °C. Synthesis of UiO-66−2COO-Ag (5). In a 20 mL scintillation vial, silver nitrate (AgNO3; 40 mg) was dissolved in MeOH (10 mL) by sonication for 10 min. UiO-66−2COOH (20 mg) was then added to the silver solution. The reaction mixture was then stirred on a hot plate at 50 °C for 20 h. The resulting brownish microcrystalline powder was centrifuged, and the supernatant was discarded. The solids were washed with MeOH for 2 d, and the solution was exchanged with fresh MeOH two times per day. The solids were collected by centrifugation and dried under dynamic vacuum at 80 °C. Antibacterial Test. The bactericidal activity of the metalated MOFs was tested against the Gram-negative strain E. coli (ATCC 25922). The MIC and MBC values were determined against E. coli using broth microdilution method following the CLSI recommendations and as described in Wiegand et al.31 Briefly, 4−5 colonies of E. coli were grown overnight (12−14 h) in 3 mL of Mueller−Hinton broth (Oxoid) at 37 °C, 120 rpm. Then, 100 μL of the overnight culture was added to 3 mL of Mueller−Hinton broth and was cultured for 3−4 h to obtain bacterial cells in the lag phase. The silver MOFs were dissolved in water and sonicated for 10 min. Then a serial dilution of silver MOFs was prepared and mixed with E. coli at a final volume of 200 μL in 96-well plates. The E. coli final concentration was between 1 × 105 and 1 × 106 CFU/ml, and the silver MOFs final concentration ranged between 1 and 200 μg/mL. Two controls were included in the experiment, which consisted of a growth control containing only the bacteria and a sterility control containing only Mueller−Hinton broth. The 96-well plates were incubated at 37 °C with minimal shaking. The optical density at 600 nm was measured using a NanoDrop 2000c spectro-photometer (Thermo Scientific) at 3, 6, 12, and 22 h. The MIC defined as the lowest concentration of silver MOF that resulted in no visible bacterial growth was read after 22 h. As for MBC, defined as the lowest concentration that resulted in more than 99.9% killing of the bacteria, it was determined by taking 50 μL aliquots from the wells that had no visual bacterial growth and were plated on LB plates. The plates were incubated at 37 °C for 16 h. All assays were performed in triplicate.

transition metals were part of the secondary building units, our reported frameworks, to the best of our knowledge, are the first postmetalated MOFs to be used as antibacterial agents. As such, the integrity of the framework should remain intact upon silver release. Indeed, SEM images for MOF incubated in Muller broth for 24 h showed no structural degradation is observed (Figure S10).

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CONCLUSION In conclusion, two Zr-based MOFs incorporating open metalbinding sites were successfully synthesized and postmetalated with Ag cations. The obtained metalated MOFs exhibited a high antibacterial activity at low silver concentrations. This method of producing antibacterial agents is novel and promising, because the highly stable Zr-MOF frameworks can be metalated with a controlled amount of Ag cations and could be regenerated to be reused. This proof of concept, we believe, will be instrumental in designing the third wave of antibacterial MOF-based compounds.

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EXPERIMENTAL SECTION

General Methods. 2,2′-Bipyridine-5,5′-dicarboxylic acid (H2bpydc) and 1,2,4,5-benzenetetracarboxylic acid, in addition to all the other reagents and solvents, were purchased from Sigma-Aldrich and used without further purification. The infrared spectroscopy (IR) spectra were recorded on a FT-IR spectrometer Thermo-Nicolet working in the transmittance mode, in the 450−3950 cm−1 range. The samples were prepared as pellets for UV−visible spectroscopy, which was performed with a JASCO V-570 UV−vis−near-IR spectrophotometer. Thermogravimetric analysis (TGA) was performed with a Netzsch TG 209 F1 Libra apparatus. The analyses were recorded in N2 flow from 30 to 800 °C at a heating rate of 3 K·min−1. Powder Xray diffraction (PXRD) patterns were collected using a Bruker D8 advance X-ray diffractometer (Bruker AXS GmbH, Karlsruhe, Germany) at 40 kV, 40 mA (1600 W) using Cu Kα radiation (k = 1.5418 Å). Scanning electron microscopy (SEM) was performed using a MIRA3 Tescan electron microscope, where the samples were first coated with a thin layer (18 nm) of gold. Nitrogen sorption measurements were performed at 77 K. Prior to the measurements, the samples were activated under dynamic vacuum at 110 °C for 6 h. Silver concentration was determined using atomic absorption spectroscopy conducted with a thermo elemental analyzer. Approximately 2 mg of the sample was digested with sonication in a mixture of water (10 mL) and HF (100 μL). The digested solution was used directly for atomic absorption test. Synthesis of UiO-67-bpydc. In a 4 mL scintillation vial, H2bpydc (10 mg, 0.04 mmol) was dissolved in 2 mL of N,N-dimethylformamide and sonicated for 10 min. Following sonication, zirconyl chloride octahydrate (ZrOCl2·8H2O; 13.0 mg, 0.04 mmol) was added to the solution. After 10 min of further sonication, formic acid (0.7 mL) was added to the solution. The reaction mixture was sonicated for a couple of minutes and then heated in an oven at 130 °C for 24 h. The resulting white microcrystalline powder was centrifuged, and the supernatant was discarded. The solids were washed with DMF for 2 d, and the solution was exchanged with fresh DMF three times per day. This was followed by washing with methanol (MeOH) for 3 d, and the solution was exchanged with fresh MeOH three times per day. The solids were collected by centrifugation and activated under dynamic vacuum at 110 °C for 12 h. Synthesis of UiO-66−2COOH. In a 20 mL scintillation vial, 1,2,4,5-benzenetetracarboxylic acid (47.0 mg, 0.184 mmol) was dissolved in 4 mL of DMF and sonicated for 10 min. Following sonication, ZrOCl2·8H2O (59.5 mg, 0.184 mmol) was added to the solution. After 10 min of further sonication, formic acid (4 mL) was added to the solution. The reaction mixture was sonicated for a couple of minutes and then heated in an oven at 130 °C for 5 h. The resulting white microcrystalline powder was purified by washing with DMF then

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ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.7b00429.

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The synthesis and characterization of UiO-67-bpydc, UiO-66−2COOH, and the silver release profile (PDF)

AUTHOR INFORMATION

Corresponding Authors

*Fax: (+961) (1)365217. E-mail: [email protected]. lb. (M.H.) *E-mail: [email protected]. (P.K.) ORCID

Pierre Karam: 0000-0003-4550-7641 Notes

The authors declare no competing financial interest. 4743

DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744

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Inorganic Chemistry

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ACKNOWLEDGMENTS We gratefully thank Prof. Y.-B. Zhang for the Pawley refinement of UiO-66-2COOH structure. We also acknowledge the funding provided by the American University Board (Nos. 103186 and 102848) and the K. Shair Central Research Science Laboratory (No. 103191).

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DOI: 10.1021/acs.inorgchem.7b00429 Inorg. Chem. 2017, 56, 4739−4744