This is an open access article published under an ACS AuthorChoice License, which permits copying and redistribution of the article or any adaptations for non-commercial purposes.
Communication pubs.acs.org/IC
Hydrogen Evolution from Water under Aerobic Conditions Catalyzed by a Cobalt ATCUN Metallopeptide Banu Kandemir,† Lenore Kubie,† Yixing Guo, Brian Sheldon, and Kara L. Bren* Department of Chemistry, University of Rochester, Rochester, New York 14627-0216, United States S Supporting Information *
ABSTRACT: The cobalt complex of an amino-terminal copper and nickel (ATCUN) motif model tripeptide (CoGGH) is shown to act as an electrocatalyst for hydrogen evolution from water near neutral pH with high Faradaic efficiency. The catalyst performance is not significantly impacted by exposure to oxygen. CoGGH represents a new class of hydrogen evolution catalyst that is straightforward to prepare and to modify.
H
ydrogen is touted as an energy-dense carbon-free fuel; however, most hydrogen is currently produced via steam reforming of hydrocarbons.1 A potentially more sustainable route to producing hydrogen is the reduction of aqueous protons. Hydrogenase enzymes catalyze rapid hydrogen evolution from water near the thermodynamic potential, but oxygen sensitivity, a lack of stability, and a low density of active sites limit their use.2 While some efforts to engineer hydrogenases to be oxygen-tolerant hydrogen producers have shown success,3 molecular catalysts using base metals have been developed as alternatives. Most of these catalysts are synthetic coordination complexes of iron, nickel, or cobalt, only a few of which are soluble in water.4−16 To enhance water solubility and functionality, hybrids between biomolecules and synthetic catalysts have been prepared.17−21 Recently, a few groups have taken the approach of reengineering biomolecules to introduce hydrogen evolution activity.18,21−24 Here, we report a related approach in which a cobalt−peptide complex that models a protein metal-binding site is developed as a water-soluble hydrogen evolution catalyst. Water-soluble cobalt complexes are promising electrocatalysts for hydrogen evolution, with reported turnover numbers (TONs) in excess of 5 × 104 (mol of catalyst)−1 and turnover frequencies (TOFs) of up to 105 (mol of catalyst)−1 h−1.22,25,26 These catalysts typically have an approximately square-planar or square-pyramidal cobalt coordination environment. Notably, peptides in the amino-terminal copper- and nickel-binding (ATCUN) motif family offer a similar coordination environment (Figure 1). The ATCUN motif is found at the N-terminus of albumins.27 It consists of three amino acids, with histidine (His) in the third position, yielding an XXH sequence. These three amino acids bind metal ions to form an N4 coordination sphere consisting of the peptide N-terminus, two deprotonated amide nitrogen atoms, and the His imidazole N(δ). The copper and nickel derivatives of this motif and its model peptides are the most commonly studied, with a focus on the catalysis of oxidative DNA cleavage and other oxidation chemistry.27−30 However, © XXXX American Chemical Society
Figure 1. CoGGH, the cobalt complex of the Gly-Gly-His ATCUN model tripeptide.
other metals also bind ATCUN peptides, including cobalt.31 In this work, we tested the hypothesis that the cobalt complex of the ATCUN model peptide Gly-Gly-His (CoGGH) would display hydrogen evolution activity in water. CoIIIGGH was prepared by combining equimolar Gly-Gly-His peptide with CoIICl2·6H2O in water at pH 8.0. A detailed description of the preparation, purification, and characterization (Figures S1−S4) is provided as Supporting Information. The diamagnetic brown product displays a UV−vis absorption spectrum with maxima at 426 and 536 nm (Figure S3), values that are slightly red-shifted from those assigned as ligand-field bands with 1A1g → 1T1g parentage for CoIIIGGH(NH3)2 (422 and 520 nm).31 The pH dependence of the absorption spectrum of the complex was monitored between pH 3 and 8, and a transition midpoint of pH 6.3 was observed (Figure S4). These data are consistent with the expected loss of cobalt coordination at acidic pH values.30 Cyclic voltammetry (CV) of CoGGH in 3-(N-morpholino)propanesulfonic acid (MOPS) buffer reveals a catalytic wave with an onset potential of ∼−1.2 V vs Ag/AgCl (Figure 2). The catalyst concentration dependence (20−136 μM, 1 M MOPS, 1 M NaCl, pH 8.0) of the voltammogram reveals a linear dependence of the current on the catalyst concentration, consistent with CoGGH acting as a molecular catalyst under these conditions (Figure S5). A concern with molecular electrocatalysts is that they may degrade to form oxides or catalytically active nanoparticles.32,33 Here, measurement of the activity using a mercury electrode rules out this complication because mercury inhibits the activity of colloidal catalysts34,35 and also forms an amalgam with cobalt.36 Received: September 18, 2015
A
DOI: 10.1021/acs.inorgchem.5b02157 Inorg. Chem. XXXX, XXX, XXX−XXX
Communication
Inorganic Chemistry
Figure 3. CPE (−1.35 V) of 35 μM CoGGH, CuGGH, NiGGH, GGH, and CoCl2 under nitrogen in 1 M MOPS and 1 M NaCl at pH 8.0. Also shown are the results of CPE of the buffer after the CoGGH-containing cell was rinsed. Data on CoGGH are only shown for the first 600 s to allow the other data to be on scale. A longer CPE experiment on CoGGH is shown in Figure S9. Figure 2. Cyclic voltammograms (0.8 V s−1) of 35 μM CoGGH as a function of the pH (labels on the right; 4.90−9.38). Samples were in 10 mM MOPS and 1 M NaCl. Inset: Plot of the peak potential (measured at −1.45 V) versus pH.
at the electrode surface is acting as the catalyst, 35 μM CoGGH was subjected to CPE at −1.35 V for 10 min, after which the working electrode compartment was gently rinsed with buffer three times and filled again with buffer. CPE then was run under the same conditions, and the minimal charge was passed (cyan trace, Figure 3). Furthermore, the observation of hydrogen evolution catalyzed by CoGGH at a mercury electrode supports CoGGH acting as a molecular catalyst because mercury is known to inhibit the activity of colloidal catalysts34,35 and mercury forms an amalgam with cobalt.36 CPE run for longer periods of time (24 h) shows that the catalyst remains active for hours but loses activity over time (Figure S9). In summary, a simple and easily assembled cobalt tripeptide catalyst operates as an electrocatalyst for hydrogen evolution from neutral-pH water with a high Faradaic efficiency. Its Faradaic efficiency is minimally impacted by the presence of air, suggesting selectivity for proton reduction. Using the half-wave potential of the catalytic wave in CV experiments as the operating potential, CoGGH operates at a ∼600 mV overpotential (pH 8, 10 mM MOPS, 1 M NaCl). This value is lower than that for a water-soluble cobalt porphyrin−peptide (∼850 mV)22 and some cobalt pentapyridine derivatives (up to ∼900 mV)7 but higher than cobalt diimine−dioxime (“cobaloxime”) catalysts, which can operate at ∼250−300 mV.6,17 One intriguing feature of the CoGGH structure is its amino group adjacent to the cobalt (Figure 1). In copper(II) ATCUN metallopeptides, this group has a pKa of close to 7,39 raising the possibility that it may act as a proton shuttle site during catalysis by CoGGH. Varying this pKa value through peptide modification thus may influence the overpotential. Indeed, the ease with which CoGGH may be modified by changing the peptide sequence40 or by introducing other modifications to the peptide30,41 makes it an attractive and versatile new type of hydrogen evolution catalyst.
The CV of CoGGH as a function of the scan rate was measured. In 1 M MOPS and 1 M NaCl, the voltammogram is nearly scan-rate-independent (Figure S6). This observation is consistent with the catalyst operating in a diffusion-controlled regime,7 although the cyclic voltammograms do not have the classic S-shape with a plateau, indicating the presence of side phenomena.37 At lower buffer concentration (10 mM MOPS), the peak current is dependent on the square root of the scan rate, indicating that it is limited by diffusion (Figures S7 and S8). Cyclic voltammograms of CoGGH were recorded as a function of the pH (4.9−9.4) in 10 mM MOPS and 1 M NaCl (Figure 2). The current reaches a maximum value at a pH of ∼6.5 (Figure 2, inset), which is consistent with a competition between enhanced CoGGH complex formation at higher pH (Figure S2) and greater proton availability for the hydrogen evolution reaction at lower pH. To detect and measure evolved hydrogen, controlled potential electrolysis (CPE) was performed on CoGGH in a sealed cell using a mercury pool electrode under either nitrogen or air, followed by analysis of the headspace gas (see the Supporting Information for experimental details and Tables S1 and S2 for the results). In a representative experiment, −1.35 V vs Ag/AgCl (1 M KCl) was applied to a 25 μM sample of CoGGH in 1 M MOPS and 1 M NaCl at pH 8.0 for 2.5 h, during which 34 μmol of hydrogen was produced and 7.26 C of charge passed. The resulting Faradaic efficiency determined was 91%, and the TON was 275; the Faradaic efficiency averaged 91 ± 3% over three runs under these conditions. Similar experiments were performed under air, and an average Faradaic efficiency of 88 ± 4% was obtained, indicating that the presence of oxygen has a minimal effect on proton reduction. Oxygen tolerance is uncommon among hydrogen-evolving catalysts22,38 but is a desirable characteristic of a component of a water-splitting system, which will produce oxygen. To determine whether CoGGH is the catalytic species, CPE was performed at −1.35 V for 1 h on 35 μM NiGGH, CuGGH, a GGH peptide, and CoCl2. Only the presence of CoGGH leads to a large increase in the charge passed relative to the background (Figure 3). As a test for whether a degradation product adsorbed
■
ASSOCIATED CONTENT
S Supporting Information *
The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.5b02157. Detailed experimental procedures, figures showing spectral and electrochemical data, and tables of electrochemical results (PDF) B
DOI: 10.1021/acs.inorgchem.5b02157 Inorg. Chem. XXXX, XXX, XXX−XXX
Communication
Inorganic Chemistry
■
(24) Slater, J. W.; Shafaat, H. S. J. Phys. Chem. Lett. 2015, 6, 3731− 3736. (25) Eckenhoff, W. T.; McNamara, W. R.; Du, P.; Eisenberg, R. Biochim. Biophys. Acta, Bioenerg. 2013, 1827, 958−973. (26) Zee, D. Z.; Chantarojsiri, T.; Long, J. R.; Chang, C. J. Acc. Chem. Res. 2015, 48, 2027−2036. (27) Harford, C.; Sarkar, B. Acc. Chem. Res. 1997, 30, 123−130. (28) Jin, Y.; Cowan, J. A. J. Am. Chem. Soc. 2005, 127, 8408−8415. (29) Joyner, J. C.; Hocharoen, L.; Cowan, J. A. J. Am. Chem. Soc. 2012, 134, 3396−3410. (30) Neupane, K. P.; Aldous, A. R.; Kritzer, J. A. Inorg. Chem. 2013, 52, 2729−2735. (31) Hawkins, C. J.; Martin, J. Inorg. Chem. 1983, 22, 3879−3883. (32) Anxolabéhère-Mallart, E.; Costentin, C.; Fournier, M.; Robert, M. J. Phys. Chem. C 2014, 118, 13377−13381. (33) Artero, V.; Fontecave, M. Chem. Soc. Rev. 2013, 42, 2338−2356. (34) Anton, D. R.; Crabtree, R. H. Organometallics 1983, 2, 855−859. (35) Paul, F.; Patt, J.; Hartwig, J. F. J. Am. Chem. Soc. 1994, 116, 5969− 5970. (36) Paklepa, P.; Woroniecki, J.; Wrona, P. K. J. Electroanal. Chem. 2001, 498, 181−191. (37) Costentin, C.; Saveant, J.-M. ChemElectroChem 2014, 1, 1226− 1236. (38) Lakadamyali, F.; Kato, M.; Muresan, N. M.; Reisner, E. Angew. Chem., Int. Ed. 2012, 51, 9381−9384. (39) Miyamoto, T.; Kamino, S.; Odani, A.; Hiromura, M.; Enomoto, S. Chem. Lett. 2013, 42, 1099−1101. (40) Kozlowski, H.; Bal, W.; Dyba, M.; Kowalik-Jankowska, T. Coord. Chem. Rev. 1999, 184, 319−346. (41) Neupane, K. P.; Aldous, A. R.; Kritzer, J. A. J. Inorg. Biochem. 2014, 139, 65−76.
AUTHOR INFORMATION
Corresponding Author
*E-mail:
[email protected]. Author Contributions †
These authors contributed equally.
Notes
The authors declare no competing financial interest.
■
ACKNOWLEDGMENTS This work was supported by National Science Foundation Grant CHE-1409929 to K.L.B. and an Elon Huntington Hooker Fellowship to B.K. The authors thank Bill Brennessel, Annada Rajbhandary, and Jalil Shojaie for technical assistance.
■
REFERENCES
(1) Chaubey, R.; Sahu, S.; James, O. O.; Maity, S. Renewable Sustainable Energy Rev. 2013, 23, 443−462. (2) Lubitz, W.; Ogata, H.; Ruediger, O.; Reijerse, E. Chem. Rev. 2014, 114, 4081−4148. (3) Murphy, B. J.; Sargent, F.; Armstrong, F. A. Energy Environ. Sci. 2014, 7, 1426−1433. (4) Chong, D. S.; Georgakaki, I. P.; Mejia-Rodriguez, R.; SanabriaChinchilla, J.; Soriaga, M. P.; Darensbourg, M. Y. Dalton T. 2003, 4158− 4163. (5) Hu, X.; Brunschwig, B. S.; Peters, J. C. J. Am. Chem. Soc. 2007, 129, 8988−8998. (6) Jacques, P.-A.; Artero, V.; Pecaut, J.; Fontecave, M. Proc. Natl. Acad. Sci. U. S. A. 2009, 106, 20627−20632. (7) Sun, Y. J.; Bigi, J. P.; Piro, N. A.; Tang, M. L.; Long, J. R.; Chang, C. J. J. Am. Chem. Soc. 2011, 133, 9212−9215. (8) Stubbert, B. D.; Peters, J. C.; Gray, H. B. J. Am. Chem. Soc. 2011, 133, 18070−18073. (9) Helm, M. L.; Stewart, M. P.; Bullock, R. M.; DuBois, M. R.; DuBois, D. L. Science 2011, 333, 863−866. (10) McCrory, C. C. L.; Uyeda, C.; Peters, J. C. J. Am. Chem. Soc. 2012, 134, 3164−3170. (11) Carroll, M. E.; Barton, B. E.; Rauchfuss, T. B.; Carroll, P. J. J. Am. Chem. Soc. 2012, 134, 18843−18852. (12) McNamara, W. R.; Han, Z.; Yin, C.-J.; Brennessel, W. W.; Holland, P. L.; Eisenberg, R. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15594−15599. (13) Valdez, C. N.; Dempsey, J. L.; Brunschwig, B. S.; Winkler, J. R.; Gray, H. B. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15589−15593. (14) Mondal, B.; Sengupta, K.; Rana, A.; Mahammed, A.; Botoshansky, M.; Dey, S. G.; Gross, Z.; Dey, A. Inorg. Chem. 2013, 52, 3381−3387. (15) Dutta, A.; Lense, S.; Hou, J.; Engelhard, M. H.; Roberts, J. A. S.; Shaw, W. J. J. Am. Chem. Soc. 2013, 135, 18490−18496. (16) Guttentag, M.; Rodenberg, A.; Bachmann, C.; Senn, A.; Hamm, P.; Alberto, R. Dalton T. 2013, 42, 334−337. (17) Bacchi, M.; Berggren, G.; Niklas, J.; Veinberg, E.; Mara, M. W.; Shelby, M. L.; Poluektov, O. G.; Chen, L. X.; Tiede, D. M.; Cavazza, C.; Field, M. J.; Fontecave, M.; Artero, V. Inorg. Chem. 2014, 53, 8071− 8082. (18) Sommer, D. J.; Vaughn, M. D.; Clark, B. C.; Tomlin, J.; Roy, A.; Ghirlanda, G. Biochim. Biophys. Acta, Bioenerg. 2015, DOI: 10.1016/ j.bbabio.2015.09.001. (19) Onoda, A.; Hayashi, T. Curr. Opin. Chem. Biol. 2015, 25, 133− 140. (20) Utschig, L. M.; Soltau, S. R.; Tiede, D. M. Curr. Opin. Chem. Biol. 2015, 25, 1−8. (21) Kandemir, B.; Chakraborty, S.; Guo, Y.; Bren, K. L. Inorg. Chem. 2015, DOI: 10.1021/acs.inorgchem.5b02054. (22) Kleingardner, J. G.; Kandemir, B.; Bren, K. L. J. Am. Chem. Soc. 2014, 136, 4−7. (23) Sommer, D. J.; Vaughn, M. D.; Ghirlanda, G. Chem. Commun. 2014, 50, 15852−15855. C
DOI: 10.1021/acs.inorgchem.5b02157 Inorg. Chem. XXXX, XXX, XXX−XXX
