Catalytic degradation of an organophosphorus agent at Zn-OH sites in a metal-organic framework

Article abstract of DOI:10.1021/acs.chemmater.0c02373

Chemical warfare agents (CWAs), and in particular organophosphorus nerve agents, still pose a significant threat to society due to their continued use despite international bans. While nature has constructed a variety of enzymes that are capable of rapidly hydrolyzing organophosphorus substrates, the poor stability of enzymes outside of buffered solutions has limited their use in practical applications, such as in filters or on protective suits. As a result, we have explored the use of metal-organic frameworks (MOFs) as robust and tunable catalytic materials in which the nodes can be tailored to resemble the active sites found in these enzymes. We identified the Zn-based MOF, MFU-4l, as a promising hydrolysis catalyst due to the presence of Zn(II)-OH groups on the nodes, which are structurally reminiscent of the active sites in carbonic anhydrase (CA), a Zn-based enzyme that has been shown to efficiently catalyze the hydrolysis of phosphate esters. Indeed, MFU-4l can rapidly hydrolyze both the organophosphorus nerve agent, GD, and its simulant, DMNP, with half-lives as low as <1 min, which is competitive with the some of best heterogeneous hydrolysis catalysts reported to date.

Full text of DOI:10.1021/acs.chemmater.0c02373

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Article
Catalytic Degradation of an Organophosphorus Agent at Zn−OH
Sites in a Metal−Organic Framework
Mohammad Rasel Mian, Timur Islamoglu,* Unjila Afrin, Subhadip Goswami, Ran Cao,
Kent O. Kirlikovali, Morgan G. Hall, Gregory W. Peterson, and Omar K. Farha*
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ABSTRACT: Chemical warfare agents (CWAs), and in particular
organophosphorus nerve agents, still pose a significant threat to society
due to their continued use despite international bans. While nature has
constructed a variety of enzymes that are capable of rapidly hydrolyzing
organophosphorus substrates, the poor stability of enzymes outside of
buffered solutions has limited their use in practical applications, such as
in filters or on protective suits. As a result, we have explored the use of
metal−organic frameworks (MOFs) as robust and tunable catalytic
materials in which the nodes can be tailored to resemble the active sites
found in these enzymes. We identified the Zn-based MOF, MFU-4l, as a
promising hydrolysis catalyst due to the presence of Zn(II)−OH groups
on the nodes, which are structurally reminiscent of the active sites in
carbonic anhydrase (CA), a Zn-based enzyme that has been shown to
efficiently catalyze the hydrolysis of phosphate esters. Indeed, MFU-4l can rapidly hydrolyze both the organophosphorus nerve
agent, GD, and its simulant, DMNP, with half-lives as low as <1 min, which is competitive with the some of best heterogeneous
hydrolysis catalysts reported to date.
sufficiently mimic the active sites in enzymes while also
exhibiting greater stability than enzymes in a wider range of
conditions. In particular, metal−organic frameworks (MOFs)
have been recognized as a versatile platform for the design of
atomically precise heterogeneous catalysts that are capable of
meeting these stringent requirements.12−18 MOFs are two- or
three-dimensional crystalline porous frameworks built from
metal-based nodes and multitopic organic linkers, and tuning
the composition of these components enables precise control
over the properties of these materials, resulting in MOFs that
offer promising solutions to a variety of global challenges,
including catalysis, gas storage and separation, water
purification, drug delivery, and sensing, among others.13,19−26
Specifically, MOFs featuring a Zr6-based node (Zr-MOFs)
have exhibited remarkable catalytic activity toward the
hydrolysis of nerve agents and nerve agent simulants, which
are molecules with similar functionality but lower toxicity, in
basic aqueous solutions.27−30 The Zr6 nodes in Zr-MOFs
feature bridging Zr−OH−Zr moieties that are similar to the
INTRODUCTION
■
While the Chemical Weapons Convention has banned the use
of chemical warfare agents (CWAs), or chemicals intended to
harm exposed people through alterations in physiological
functions, the use of CWAs has remained prevalent in recent
years.1−3 In particular, organophosphorus nerve agents
comprise a class of CWAs that are some of the most toxic
chemicals known to humanity, and their continued worldwide
use despite international prohibition has warranted the
development of materials capable of rapidly detoxifying these
nerve agents.4 Nature has elegantly produced a variety of
enzymes that can effectively hydrolyze organophosphorus
substrates, and while their structures differ greatly, these
enzymes all feature Lewis acidic metal−oxy/hydroxy species
that function as active sites for catalysis.5−8 For example, the
enzyme phosphotriesterase (PTE) contains an active site in
which two Zn(II) ions are bridged by a hydroxyl anion,
enabling PTE to rapidly hydrolyze organophosphorus nerve
agents, such as sarin, cyclosarin, and soman.9−11 Although
these enzymes exhibit great performance for the catalytic
hydrolysis of nerve agents, the poor stability of enzymes
outside of buffered solutions and after long-term storage has
precluded their use in practical applications, such as coatings
on protective suits or on filters used in masks.
Received: June 6, 2020
Revised: July 20, 2020
Drawing inspiration from biology, researchers sought to
develop robust metal oxide-based materials that could
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Figure 1. Hydrolysis reaction of (a) the phosphonate-based nerve agent simulant DMNP (dimethyl (4-nitrophenyl) phosphonate) and (b) the real
nerve agent GD (O-pinacolyl methylphosphonofluoridate). (c) Structural representation of MFU-4l. (d) Cl− ion is replaced with OH− after base
treatment. (e) Comparison between the active site in MFU-4l and carbonic anhydrase (CA). Brown, Zn; green, Cl, gray, C; blue, N; and red, O.
Hydrogen atoms are omitted for clarity.
Lewis acidic active sites found in enzymes such as PTE, and
strong Zr(IV)−O bonds between the Zr6 node and carboxylate
linkers result in excellent chemical and thermal stability
properties for Zr-MOFs.31 Through systematic investigations,
we determined that greater accessibility to the Lewis acidic Zr6
nodes (e.g., larger pore apertures, lower node connectivities,
and smaller particle sizes) generally results in the faster
catalytic hydrolysis of organophosphorus substrates,32 and our
team has recently demonstrated that Zr-MOF/textile compo-
sites are capable of hydrolyzing nerve agents under practical
conditions using only water that is present as humidity.33 As
part of our continued efforts to improve the performance of
organophosphorus hydrolysis catalysts, we extended our
investigation to include other stable MOFs with Lewis acidic
sites to complement the highly capable Zr- and Ce-based
MOFs we studied previously.27,34 Specifically, we drew
inspiration from the carbonic anhydrase (CA) class of
metalloenzymes.35,36 In addition to CO2 hydration, CAs are
also capable of hydrolyzing esters and phosphonate esters with
performance similar to that of other enzymes, such as esterase
phosphatase.37 Hydrolysis in CAs occurs at the Zn(II)−OH
active sites (Figure 1e) in which the electronegative OH−
group acts as a nucleophile that attacks the partially
electropositive central atom of the ester or phosphonate
ester (i.e., carbonyl or phosphorus atom), forming an
intermediate from which the C−O or P−O bond is
subsequently cleaved.38 However, the lack of thermal stability,
long-term stability, and high cost of CAs limit their practical
use. Therefore, we considered MOFs that contain nodes with
accessible Zn(II)−OH groups coordinated to nitrogen-based
ligands as potential CA mimics that may exhibit similar
reactivity to these enzymes with improved thermal and
chemical stability.
In this work, we investigate the Zn triazole-based MOF
MFU-4l, which is constructed with 6-connected Zn5 nodes and
bis(1H-1,2,3-triazolo-[4,5-b],[4′,5′-i])dibenzo-[1,4]-dioxin
(H2-BTDD) linkers (Figure 1c).39 Four of the Zn(II) ions are
tetrahedrally coordinated by three linkers and one Cl− anion,
and one Zn(II) ion is octahedrally coordinated by six BTDD2−
linkers. MFU-4l exhibits good chemical stability in basic
aqueous solutions, and spectroscopic studies reveal that under
these conditions the Cl− ions coordinated to Zn(II) in the
parent MFU-4l are rapidly replaced with OH− groups, forming
the Zn(II)−OH group that is reminiscent of the active sites
found in CAs. Importantly, MFU-4l is an extremely effective
catalyst for the hydrolysis of the nerve agent GD and the nerve
agent simulant DMNP in basic aqueous solutions with half-
lives of 3.3 and <1 min, respectively, which are among the best
for MOF-based catalysts employed under similar conditions,
thus paving the way toward a new class of organophosphorus
nerve agent hydrolysis catalysts.
EXPERIMENTAL SECTION
■
MFU-4l was prepared through the solvothermal synthesis in
dimethylformamide (DMF) at 140 °C for 18 h (see the Supporting
Information for more details). Bulk phase purity of the activated
materials was confirmed through powder X-ray diffraction (PXRD)
analysis as the obtained experimental pattern is consistent with the
simulated pattern (Figure 2a). Scanning electron microscope (SEM)
images reveal a cubic morphology with particle sizes ranging from 300
to 800 nm, as expected from the cubic unit cell of MFU-4l (Figure
S1). The Brunauer−Emmett−Teller (BET) area and pore volume are
calculated to be 3430 cm2 g−1 and 1.13 cm3 g−1, respectively, which
were obtained from N2 isotherms collected at 77 K (Figure 2b).
B
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conducted with MFU-4l powders without any chemical
modification. Initial hydrolysis reactions were performed with
6 mol % catalyst loading in pH 10.5 solution at room
temperature by using N-ethylmorpholine (EM) as the base
(see the Supporting Information for more details), and 31P
NMR spectroscopy was used to monitor the reaction progress
(Figure 3a). As the reaction proceeds, the peak around −4.4
Figure 2. (a) PXRD patterns of MFU-4l (black is simulation and red
is experimental) and postcatalysis samples of MFU-4l with either EM
(blue) or PAMAM-1.0 (pink). (b) N2 isotherms at 77 K for MFU-4l
(red) and after soaking the MFU-4l in EM solution for 20 min (blue).
Hydrolysis of DMNP. Catalysis experiments were performed by in
situ 31P NMR spectroscopy at room temperature. 1.9 mg (6 mol %) of
MFU-4l was added to 1.05 mL of EM solution (0.05 mL of EM (0.4
mmol), 0.9 mL of deionized water, and 0.1 mL of D2O) in a 1.5 mL
dram vial. The resulting mixture was stirred for 2 min to disperse the
MOF powder. DMNP (4.0 μL, about 6.2 mg) was added to this
suspension and swirled for 10 s. The reaction mixture was then
transferred to an NMR tube, and the spectrum was immediately
measured; the first data point was collected as fast as possible after the
start of the reaction. The reaction progression was monitored by 31P
NMR spectroscopy via the formation of a dimethyl phosphate anion.
For reactions with PAMAM-1.0, the amount of dendrimer was based
on the same molar amount of nitrogen compared to EM (0.4 mmol).
The volume of PAMAM-1.0 is 132 μL.
Hydrolysis of GD. 1.9 mg (6 mol %) of MFU-4l was added to
1.05 mL of EM or PAMAM-1.0 buffer in a 1.5 mL dram vial. The
resulting mixture was stirred for 2 min to disperse the MOF powder.
GD (4.4 μL, 25 μmol) was added to this suspension. The reaction
progression was monitored by 31P NMR spectroscopy via the
formation of pinacolyl methylphosphonic acid (PMPA).
Figure 3. (a) 31P NMR spectra obtained from the hydrolysis of
DMNP (δ = −4.4 ppm) to the dimethoxy phosphate anion (δ = 2.8
ppm) with the Zr5 node and MFU-4l with EM and PAMAM-1.0 as
the base at different time points. (b) Kinetic profiles of DMNP
hydrolysis with MFU-4l using 6 mol % catalyst loading in the
presence of EM (blue) and PAMAM-1.0 (pink) as the base.
ppm that corresponds to DMNP disappears, and a new peak
appears at 2.8 ppm, indicating the formation of the dimethyl
phosphate anion;32,41 the relative ratios obtained from
integrating these two peaks are used to construct kinetic
profiles (Figure 3b). When MFU-4l is employed as a catalyst
under these conditions, more than 80% of DMNP is converted
to the benign phosphate product in under 3 min, and a first-
order kinetic equation was used to calculate the initial reaction
rate constants and half-lives.40 Notably, the calculated half-life
(t1/2) for hydrolysis of DMNP is <1 min, which is comparable
to those of the some of the best Zr-MOF hydrolysis catalysts,
MOF-808 and NU-901 (t1/2 = <0.5 and 1 min, respectively,
Table 1).41,42 Additionally, decreasing the amount of MFU-4l
to 3 mol % results in a t1/2 of 1.8 min for DMNP hydrolysis
(Figure S2), and the initial rate constant was calculated to be
0.24 0.01 min−1 (Figure S3).
RESULTS AND DISCUSSION
■
After confirming the structural purity and permanent porosity
of MFU-4l, we evaluated the catalytic activity of MFU-4l
against the hydrolysis of the nerve agent simulant dimethyl (4-
nitrophenyl)phosphate (DMNP, Figure 1a). We hypothesized
that under catalytically relevant conditions in basic aqueous
solutions, Cl− ions would be replaced with OH− groups in situ
to form Zn(II)−OH sites, so catalytic reactions were
Recently, we studied the performance of Zr-MOF hydrolysis
catalysts when the volatile EM was replaced with a less volatile
C
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was observed after 15 min (Figure 3a); around 20% conversion
was observed 3 h later (Figure S7) which can be attributed to
the Zn(II)−OH sites on the surface of crystals. These results
suggest that MFU-4l acts as a heterogeneous catalyst and that
the ditopic BTDD linker yields a highly porous network that
provides sufficient distance between the Zn5 active sites in
MFU-4l to enable DMNP access, highlighting the importance
of porosity in heterogeneous catalysis.
Table 1. Comparison between the Performance of Selected
MOF Catalysts for the Hydrolysis of DMNP and GD
a
MOF
MFU-4l
MOF-808
NU-1000-dehy
NU-1000
NU-901
UiO-66
UiO-66-NH2
NU-1600
Spirof-MOF-b
simulant, real agent
t1/2 (min)
ref
DMNP, GD
DMNP
DMNP
DMNP, GD
DMNP
DMNP
DMNP
DMNP
DMNP
<1, 3.3
this work
b
<0.5
42
32
32
41
43
44
45
46
1.5
15, 3
1
45
1
As previous studies indicate that Zn(II)−OH sites (pKa =
9.0
0.1) are the reactive sites for the hydrolysis of
organophosphorus compounds,47 the observed hydrolytic
reactivity for MFU-4l suggests the Cl− capping ligands on
the parent MFU-4l are replaced with OH− ligands under the
basic reaction conditions. We investigated the influence of pH
on the catalytic activity observed for MFU-4l, finding that the
reactivity is comparable in pH 10.5 and 9.5 solutions, but a
significant decrease in reactivity is observed when the pH of
the solution is reduced to 8.5 (Figure S4). The difference in
reactivity is much more pronounced at the initial time points of
each reaction relative to when the reactions plateau, suggesting
the rate of replacement of Cl− ligands by OH− ligands occurs
much faster at pH 9.5 and above.
1
1.8
a
General conditions: 6 mol % MOF loading, 0.4 M EM, pH 10−10.5,
b
H2O. 1.5 mol % catalyst.
base, which is an important consideration for the use of these
catalysts in practical applications, such as in protective suits or
in filters used in masks, and found that the use of dendritic and
polymeric amine bases results in nearly identical peformance.41
Among these bases, the PAMAM-1.0 dendrimer achieved the
best performance with the Zr-MOF system. On the basis of
these previous results, we decided to test the PAMAM-1.0
dendrimer in DMNP hydrolysis reactions with MFU-4l,
finding that t1/2 = <1 min and that the kinetic profile for this
reaction is comparable to that of the reaction performed with
EM (Figure 3b).
To investigate the stability of MFU-4l following catalytic
reactions, MFU-4l was filtered from the postcatalysis reaction
mixture and dried after washing with methanol. The PXRD
pattern obtained for this sample is preserved, which confirms
the structural integrity of MFU-4l (Figure 2a). As a further
control, we prepared the complex [Zn5Cl4(bnz)6] (bnz =
benzotriazole), and single-crystal X-ray diffraction studies
indicate that this complex has similar Zn5 nodes to those
found in MFU-4l (Figure S5a). Unlike the porous framework
in MFU-4l, the dense packing of [Zn5Cl4(bnz)6] did not reveal
any accessible internal void space (Figure S5b). Both crystals
and ground powders of [Zn5Cl4(bnz)6] were used for DMNP
hydrolysis under the reaction conditions previously described,
but no measurable reactivity toward the hydrolysis of DMNP
To investigate the kinetics of Cl−/OH− ligand exchange for
this system, MFU-4l was soaked in aqueous solutions of EM at
pH 10.5 for 5, 10, 15, and 20 min. Solids were filtered and
washed with acetone three times, then dried at 100 °C under
vacuum for 60 min, and finally characterized by using multiple
techniques. First, diffuse reflectance infrared Fourier transform
spectroscopy (DRIFTS) was employed to monitor the
presence of hydroxyl anions. According to the DRIFTS spectra
presented in Figure 4a,b, a new band appears at 3700 cm−1 in
all samples treated in EM solution that was not initially present
in the DRIFTS spectrum obtained for the parent MFU-4l,
which is attributed to the hydroxyl stretches of Zn(II)−OH.
The intensity of this peak does not change significantly with
time, suggesting that near complete conversion from Cl− to
OH− occurs within 5 min.
Next, X-ray photoelectron spectroscopy (XPS) was used to
quantify the amount of Cl present in each sample. A broad
peak around 198 eV is observed for the parent MFU-4l, which
Figure 4. DRIFTS spectra (a, b) and XPS (c) core spectra for Cl 2p scans taken at different time points after treatment of MFU-4l in EM solutions
at room temperature.
D
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corresponds to binding energy of 2p core electrons in Cl
(Figure 4c). The peak could be separated into doublets (2p3/2
and 2p1/2) by using a Gaussian−Lorentzian line fitting. After
soaking the sample in EM solution for 5 min, no detectable
peak beyond background noise is observed in the region,
indicating that all Cl− ions have been replaced with OH− ions
by this time point. Furthermore, EDX spectra obtained for
MFU-4l show 4.8 wt % Cl, whereas the amount of Cl is found
to be 0.4 wt % and below after soaking MFU-4l in EM for 5,
10, 15, and 20 min (Figure S8); the small amount of Cl
observed in the EDX spectra is due to the background noise
(Figures S9 and S10). Finally, the N2 adsorption isotherm
collected for a sample of MFU-4l soaked in EM solution for 20
min shows a BET area of 3350 cm2 g−1, which is comparable to
the BET area of 3430 cm2 g−1 obtained for the parent MFU-4l
(Figure 2b). SEM images reveal that the cubic morphology of
MFU-4l is maintained even after soaking in EM solution
(Figure S1). Overall, all spectroscopic studies indicate that
upon soaking in EM solutions at pH 10.5 the Cl− ligands are
replaced with OH− groups within 5 min, at which point most
of the DMNP is consumed, suggesting that the Zn(II)−OH
sites are the active sites for the hydrolysis of DMNP.
After determining that MFU-4l is capable of rapidly
hydrolyzing DMNP in basic aqueous solutions, we decided
to investigate the reactivity of MFU-4l toward the actual nerve
agent soman, also known as GD. Hydrolysis reactions were
conducted using 6 mol % MFU-4l as the catalyst and either
EM or PAMAM-1.0 as the base, and progress of the reaction
was monitored via 31P NMR spectroscopy (Figure S11). As the
reaction proceeds, two doublets around 31 and 37 ppm that
correspond to GD decrease in intensity, and a singlet assigned
to the nontoxic hydrolysis product, pinacolyl methyl-
phosphonic acid (PMPA), appears at 25 ppm.32,33 The
hydrolytic reactivity of MFU-4l toward GD in solutions of
EM and PAMAM-1.0 is comparable to that observed for
DMNP hydrolysis, with calculated half-lives of 3.3 and 4.0 min,
respectively (Figure 5), and the initial rate constant for GD
CONCLUSION
■
We have demonstrated that MFU-4l, a Zn-triazole-based
MOF, can catalyze the rapid hydrolysis of the organo-
phosphorus nerve agent, GD, and its simulant, DMNP, with
half-lives of 3.3 and <1 min, respectively. The combination of
soft Lewis acidic Zn(II) and soft Lewis basic triazole-based
building blocks of MFU-4l yields a heterogeneous catalyst that
is stable under basic conditions. Spectroscopic studies reveal
that the in situ ligand exchange from Cl− to OH− occurs within
minutes to form the Zn(II)−OH species, which resemble the
active site of the CA enzyme. Reactions performed under
analogous conditions by using the nonporous, molecular Zn5
cluster [Zn5Cl4(bnz)6] show negligible hydrolysis of DMNP,
emphasizing the importance of organophosphorus substrate
accessibility to the internal active sites in MFU-4l for efficient
catalysis to occur. We anticipate that these results will pave the
way toward the design of even more efficient Zn-azolate-based
heterogeneous catalysts for the hydrolysis of organophospho-
rus nerve agents.
ASSOCIATED CONTENT
* Supporting Information
The Supporting Information is available free of charge at
https://pubs.acs.org/doi/10.1021/acs.chemmater.0c02373.
■
sı
Instrumentation, syntheses of MFU-4l and
[Zn5Cl4(bnz)6], hydrolysis procedure details, SEM
image, crystal structure and crystallographic data for
[Zn5Cl4(bnz)6], EDX, SEM-EDX mapping, XPS anal-
ysis, and NMR spectra (PDF)
Crystallographic data for [Zn5Cl4(bnz)6] (CIF)
AUTHOR INFORMATION
Corresponding Authors
■
Timur Islamoglu − International Institute of Nanotechnology
and Department of Chemistry, Northwestern University,
Evanston, Illinois 60208, United States; orcid.org/0000-
0003-3688-9158; Email: timur.islamoglu@northwestern.edu
Omar K. Farha − International Institute of Nanotechnology and
Department of Chemistry and Department of Chemical &
Biological Engineering, Northwestern University, Evanston,
Illinois 60208, United States; orcid.org/0000-0002-9904-
9845; Email: o-farha@northwestern.edu
Authors
Mohammad Rasel Mian − International Institute of
Nanotechnology and Department of Chemistry, Northwestern
University, Evanston, Illinois 60208, United States;
orcid.org/0000-0002-3034-8054
Unjila Afrin − International Institute of Nanotechnology and
Department of Chemistry, Northwestern University, Evanston,
Illinois 60208, United States
Subhadip Goswami − International Institute of Nanotechnology
and Department of Chemistry, Northwestern University,
Evanston, Illinois 60208, United States; orcid.org/0000-
0002-8462-9054
Figure 5. Hydrolysis profile of GD with MFU-4l using 6 mol %
catalysts loading in the presence of EM (blue) and PAMAM-1.0
dendrimer (pink).
Ran Cao − International Institute of Nanotechnology and
Department of Chemistry, Northwestern University, Evanston,
Illinois 60208, United States
Kent O. Kirlikovali − International Institute of Nanotechnology
and Department of Chemistry, Northwestern University,
Evanston, Illinois 60208, United States; orcid.org/0000-
0001-8329-1015
hydrolysis in EM solution was calculated to be 0.18
0.03
min−1 (Figure S12). Overall, these data place MFU-4l among
the most active heterogeneous GD hydrolysis catalysts
reported to date under these conditions.27
E
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Morgan G. Hall − CCDC Chemical Biological Center, Aberdeen
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Gregory W. Peterson − CCDC Chemical Biological Center,
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Complete contact information is available at:
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Notes
The authors declare no competing financial interest.
ACKNOWLEDGMENTS
■
The authors gratefully acknowledge support from the Defense
Threat Reduction Agency (HDTRA1-18-1-0003). Use was
made of the IMSERC X-ray facility at Northwestern
University, which has received support from the Soft and
Hybrid Nanotechnology Experimental (SHyNE) Resource
(NSF ECCS-1542205), the State of Illinois, and the Interna-
tional Institute for Nanotechnology (IIN). This work made use
of the EPIC facility of Northwestern University’s NUANCE
Center, which has received support from the Soft and Hybrid
Nanotechnology Experimental (SHyNE) Resource
(NSFECCS-1542205), the MRSEC program (NSF DMR-
1720139) at the Materials Research Center, the International
Institute for Nanotechnology (IIN), the Keck Foundation, and
the State of Illinois through the IIN. K.O.K. gratefully
acknowledges support from the IIN Postdoctoral Fellowship
and the Northwestern University International Institute for
Nanotechnology.
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