Kinetics and mechanistic analysis of an extremely rapid carbon dioxide fixation reaction Deguang Huanga, Olga V. Makhlynetsb, Lay Ling Tanc, Sonny C. Leec, Elena V. Rybak-Akimovab, and R. H. Holma,1 aDepartment of Chemistry and Chemical Biology, Harvard University, Cambridge, MA 02138; bDepartment of Chemistry, Tufts University, Medford, MA 02155; and cDepartment of Chemistry, University of Waterloo, Waterloo, ON, Canada N2L3G1 Contributed by R. H. Holm, November 23, 2010 (sent for review October 30, 2010) Carbon dioxide may react with free or metal-bound hydroxide to afford products containing bicarbonate or carbonate, often cap- tured as ligands bridging two or three metal sites. We report the kinetics and probable mechanism of an extremely rapid fixation re- action mediated by a planar nickel complex ½NiIIðNNNÞðOHÞ1− con- taining a tridentate 2,6-pyridinedicarboxamidate pincer ligand and a terminal hydroxide ligand. The minimal generalized reaction is → M-OH þ CO2 M-OCO2H; with variant M, previous rate constants are ≲103 M−1 s−1 in aqueous solution. For the present bimolecular reaction, the (extrapolated) rate constant is 9.5 × 105 M−1 s−1 in N, N′-dimethylformamide at 298 K, a value within the range of k ∕K ≈ 5– 8 −1 −1 cat M 10 10 M s for carbonic anhydrase, the most efficient catalyst of CO2 fixation reactions. The enthalpy profile of the fixation reaction was calculated by density functional theory. The initial event is the formation of a weak precursor complex between the Ni-OH group and CO2, followed by insertion of a CHEMISTRY CO oxygen atom into the Ni-OH bond to generate a four center 2 — Me2 η2 Fig. 1. Absorption spectra in DMF: black trace ðEt4NÞ½NiðpyN2 ÞðOHÞ; Nið -OCO2HÞ transition state similar to that at the zinc site in blue trace—after bubbling CO2 through the solution for 2 min; red trace carbonic anhydrase. Thereafter, the Ni-OH bond detaches to afford Me2 —after vigorous bubbling of N2 through the solution of ðEt4NÞ½NiðpyN Þ η1 2 the Nið -OCO2HÞ fragment, after which the molecule passes ðHCO3Þ (blue trace) for 20 min. (Inset) Kinetics trace acquired at 450 nm and A A ΔA −k t through a second, lower energy transition state as the bicarbonate 233 K overlaid with a single exponential fit to ¼ ∞ þ expð obs Þ, ligand rearranges to a conformation very similar to that in the where A∞ is the absorbance after complete reaction, ΔA ¼ A0 − A∞, A0 k crystalline product. Theoretical values of metric parameters and is the initial absorbance, and obs is the observed rate constant. Reactant Me2 1− 0 1 1 activation enthalpy are in good agreement with experimental concentrations: f½NiðpyN2 ÞðOHÞ g¼ . mM, ½CO2¼ mM. values [ΔH‡ ¼ 3.2ð5Þ kcal∕mol]. Several features of the CO2 fixation reaction 1 are noteworthy. ∣ – ∣ nickel hydroxide carbon dioxide bicarbonate conversion The reactant is a terminal hydroxide species affording a uniden- reaction mechanism 1 tate bicarbonate (η -OCO2H) product. Far more common is the II reaction of bridged M 2ðμ-OHÞ1;2 precursors to afford binuclear ecent research in this laboratory has been directed toward or occasional trinuclear products bridged by carbonate utilizing Rthe attainment of synthetic analogues of the NiFe3S4 active two or three oxygen atoms (4–9). A second feature is the appar- site of the enzyme carbon monoxide dehydrogenase (1, 2), which þ − ently fast reaction rate, given that CO2 comprises only 0.039 vol catalyzes the interconversion reaction CO2 þ 2H þ 2e ⇌ % of the atmosphere. Although fixation of atmospheric CO2 by CO H2O. In the course of this work, we have prepared binuc- þ metal hydroxide species has been previously observed (4, 5, 7, 10), lear NiII∕FeII bridged species with the intention of simulating including with NiII (7, 11–13), no quantitation of reaction rates the Ni…Fe component of the enzyme site that is the locus of and analysis of reaction mechanism are available. The fixation substrate binding, activation, and product release (3). The nickel of carbon dioxide, whereby this greenhouse gas is rendered in site in the binuclear species has been prepared separately in the Me2 1− chemically combined forms, is of current environmental and form of the planar hydroxide complex ½NiðpyN2 ÞðOHÞ con- taining a N,N′-2,6-dimethylphenyl-2,6-pyridinedicarboxamidate biological interest. Fixation leads to utilization of the compound dianion. Whereas bridging hydroxide ligation is common, term- as a renewable carbon resource in the formation of useful organic inal binding is not and in general is stabilized in divalent metal compounds, ideally in catalytically efficient systems (14, 15). complexes by hydrogen bonding or by steric shielding, as is the Atmospheric capture of CO2 allows its sequestration by various case here. As reported recently (3), exposure of a solution of methods including conversion to metal carbonates (16). In biol- Me2 1− ½NiðpyN2 ÞðOHÞ to the atmosphere results in an instanta- ogy, the ubiquitous Zn(II) enzyme carbonic anhydrase catalyzes ⇌ − þ neous color change from red to red–orange. This results in the fixa- the reversible hydration reaction CO2 þ H2O HCO3 þ H , Me2 1− tion of CO2 as the bicarbonate complex ½NiðpyN2 ÞðHCO3Þ which among other functions leads to the removal of CO2 from accompanied by the spectral changes in Fig. 1. tissues in the mammalian respiratory process. Given the fore- Author contributions: D.H., S.C.L., and R.H.H. designed research; D.H., O.V.M., L.L.T., and S.C.L. performed research; S.C.L. and E.V.R.-A. analyzed data; and S.C.L., E.V.R.-A., and R.H.H. wrote the paper. The authors declare no conflict of interest. 1To whom correspondence should be addressed. E-mail: [email protected]. This article contains supporting information online at www.pnas.org/lookup/suppl/ doi:10.1073/pnas.1017430108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1017430108 PNAS Early Edition ∣ 1of6 Downloaded by guest on September 28, 2021 Table 1. Observed rate constants as a function of water Table 2. Kinetics parameters for carbon dioxide fixation with Me2 1− content in DMF ½NiðpyN2 ÞðOHÞ in DMF solutions II k −1 ΔH‡ ΔS‡ k k † Water, equiv vs Ni obs,s , , 2,* 228 K, 2, 298 K, ∕ ∕ −1 −1 −1 −1 0 88.2 Experiment kcal mol cal mol K M s M s ‡ 5 800 82.4 Variable CO2 4.7(1.5) −15(5) 1.04ð7Þ × 10 — 5 5 1600 72.6 Constant CO2 3.2(5) −20(3) 1.45ð1Þ × 10 9.5 × 10 3200 49.7 *Experimental value. Kinetics traces at 450 nm and 218 K were fitted to the single †Extrapolated value. A A ΔA −kt ‡ k k exponential ¼ ∞ þ expð Þ defined in Fig. 1. Concentration See Fig. 2; 2 at each temperature was determined from the slopes of obs vs Me2 1− 0 1 1 0 of reactants: f½NiðpyN2 ÞðOHÞ g¼ . mM, ½CO2¼ . mM. [CO2] plots (data in SI Text). k Each obs is the average of eight runs. on NiII concentration. Consequently, for reaction 1, rate ¼ going factors, we have determined the kinetics of reaction 1 and k Me2 1− k k 2f½NiðpyN2 ÞðOHÞ g½CO2. A full set of obs and 2 data examined its mechanism with the aid of theoretical calculations. is available (SI Text). Second-order rate constants at 228 K and Results and Discussion 298 K are given in Table 2 together with activation parameters obtained from the Eyring equation plotted in Fig. 3. The data Kinetics of CO Fixation. 2 The kinetics of reaction 1 were determined plotted are from the experiment with constant ½CO2¼1 mM. in dimethylformamide (DMF) solutions by stopped-flow spectro- The negative activation entropies are consistent with an associa- – photometry at 218 243 K. As seen in Fig. 1, the absorption tive transition state. Me2 1− spectrum of ½NiðpyN2 ÞðOHÞ contains a peak at 411 nm Table 3 contains a summary of second-order rate constants for Me2 and a shoulder near 490 nm, whereas the product ½NiðpyN2 Þ CO2 fixation at ambient temperature, which may be compared 1− 5 −1 −1 ðHCO3Þ presents maxima at 300 and 381 nm. The reaction was with the extrapolated value of k2 ¼ 9.5 × 10 M s at 298 K for followed by absorbance changes at 450 nm under conditions of reaction 1. These data were obtained in aqueous solution in a ≥10 variable and constant CO2 concentrations ( -fold excess of pH range sufficient to deprotonate coordinated water and thus CO2 with respect to Ni). In treating the low-temperature absor- refer to the minimal reaction M-OH þ CO2 → M-OCO2H. The zþ bance data, no evidence of a preequilibrium was found. A typical synthetic reactants ½LnM-OH are primarily octahedral com- single exponential fit of the data (233 K) in the presence of a plexes of CoIII and five-coordinate ½ZnðcyclenÞðOHÞ1þ, perhaps 10-fold excess of CO2 is included as an inset, from which the the most successful kinetics mimic of the carbonic anhydrase site k pseudo-first-order rate constant obs can be evaluated. The influ- (17). Of the multitude of kinetics information available for car- ence of water on the reaction rate was investigated under the bonic anhydrase, data for the human enzymes I, II, and III are conditions of Table 1. The possibility that CO2 is hydrated by selected because of the availability of k and K data. It is evi- ⇌ cat M small amounts of water in DMF by the reaction CO2 þ H2O dent that the rate constant for reaction 1 enters the domain of − þ Me2 HCO3 þ H and that bicarbonate reacts with ½NiðpyN2 Þ ≳102 1− carbonic anhydrase kinetics and is faster than any metal- ðOHÞ to form a carbonate complex and water appears remote.