Proton-Coupled Electron Transfer Drives Long-Range Proton

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Proton-coupled electron transfer drives longrange proton translocation in bioinspired systems Emmanuel Odella, Brian L. Wadsworth, Sabrina Jimena Jimena Mora, Joshua J. Goings, Mioy T. Huynh, Devens Gust, Thomas A. Moore, Gary F. Moore, Sharon Hammes-Schiffer, and Ana L. Moore J. Am. Chem. Soc., Just Accepted Manuscript • DOI: 10.1021/jacs.9b06978 • Publication Date (Web): 07 Aug 2019 Downloaded from pubs.acs.org on August 7, 2019

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Journal of the American Chemical Society

Proton-coupled electron transfer drives long-range proton translocation in bioinspired systems Emmanuel Odella,§‡ Brian L. Wadsworth,§‡ S. Jimena Mora,§‡ Joshua J. Goings,†‡ Mioy T. Huynh,† Devens Gust,§ Thomas A. Moore,§ Gary F. Moore,§* Sharon Hammes-Schiffer,†* and Ana L. Moore.§* §

School of Molecular Sciences, Arizona State University, Tempe, Arizona 85287-1604, United States. †

Department of Chemistry, Yale University, New Haven, Connecticut 06520-8107, United States.

enzymes, PCET can also provide the lowest-energy reaction pathway for breaking and making chemical bonds in myriad biochemical reactions.3-9

ABSTRACT: Proton-coupled electron transfer (PCET) combines the movement of fundamental charged species to form an essential link between electron- and proton-transport reactions in bioenergetics and catalysis in general. The length scale over which proton transport may occur within PCET processes and the thermodynamic consequences of the resulting proton chemical potential to the oxidation reaction driving these PCET processes have not been generally established. Here we report the design of bioinspired molecules that employ oxidation-reduction processes to move reversibly two, three, and four protons via a Grotthusstype mechanism along hydrogen-bonded networks up to ~16 Å in length. These molecules are composed of benzimidazole moieties linking a phenol to the final proton acceptor, a cyclohexylimine. Following electrochemical oxidation of the phenol, the appearance of an infrared band at 1660 cm-1 signals proton arrival at the terminal basic site. Switching the electrode potential to reducing conditions reverses the proton translocation and resets the structure to the initial species. In addition to mimicking the first step of the iconic PCET process used by the Tyrz-His190 redox relay in photosystem II to oxidize water, this work specifically addresses theoretically and experimentally the length scale over which PCET processes may occur. The thermodynamic findings from these redox-driven, bioinspired “proton wires” have implications for understanding and rationally designing pumps for the generation of proton-motive force in artificial and reengineered photosynthesis, as well as for management of proton activity around catalytic sites, including those for water oxidation and oxygen reduction.

Scheme 1. Molecular structures of benzimidazole-phenol (BIP) derivatives and their oxidation products.

Electrons and protons move in specific ways under gradients of chemical potential to perform the most fundamental processes of all living cells. These processes include the generation of protonmotive force (PMF, the difference in electrochemical potential of protons across a membrane), which provides the energy to maintain living systems in a stable state far from equilibrium.1-2 Proton-coupled electron transfer (PCET) is a mechanism for reversibly translating chemical potential energy from redox processes to PMF and vice versa. When choreographed by

On the left, compounds 1, 2, 3 and 4 designed to explore E1PT, E2PT, E3PT and E4PT (generically EnPT) processes, respectively. On the right, products of the electrochemical oxidation of the phenol coupled with one (1’), two (2’), three (3’) and four (4’) proton transfers. The hydrogen atoms involved in the PCET reactions are labeled in orange and the EnPT processes are color coded as in Figures 1 and 2.

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Depending on the solvent, compounds 1 and 2 may exist as mixtures of isomers due to both the 1,3-tautomerism of imidazole and rotation around the bond connecting the benzimidazole and the phenol moieties. In the case of 2, in a non-polar solvent such as CDCl3, only one of these isomers, the closed cis enol23, acquires the hydrogen bond network necessary for intramolecular proton transfers to take place upon phenol oxidation. As the number of benzimidazole units increases from 2 to 4 (Scheme 1), the number of possible isomers in solution increases as well. For compounds analogous to 4 with a para-substituted phenyl group instead of the cyclohexyl group attached to the imine nitrogen, the presence of at least three isomers can be clearly detected from the 1H NMR spectra in the low field region in CDCl3 (Figure S17). However, the 1H NMR spectrum drastically changes indicating that a single isomer predominates in CDCl3 solution when the cyclohexylimine moiety is used as the final proton acceptor. We propose the stronger basicity of the imine nitrogen in 4 compared with that of the analogous phenylimine derivatives strengthens the terminal hydrogen bond, favoring the conformation where the hydrogen bond network extends across the molecule as shown in Scheme 1; this highlights the importance of targeting an appropriate terminal

A progression of four molecules in which electrochemical oxidation of the phenol initiates the displacement of the phenolic proton is shown in Scheme 1. In each case, the phenol models Tyrz and the benzimidazole models His190 of photosystem II.10-13 Proton transfer to the attached imidazole and other proton acceptors have been extensively characterized.13-18 Additionally, in 1 the amide serves as a model for Asn298.11 In photosynthesis, Asn298 is hydrogen bonded to His190, but proton transfer from the protonated His190 to it remains controversial.19 The amide in 1 cannot accept a proton due to an unfavorable pKa, so that the benzimidazolium ion 1’ is the final PCET product.20 In compounds 2, 3 and 4, protons translocate across the benzimidazole moieties to the terminal cyclohexylimine (vide infra). In 1, the one-electron one-proton transfer process is known as an E1PT process. In 2, a cyclohexylimine hydrogen bonded to the distal NH of the benzimidazole provides a network for proton translocation to the imine site. Because a one-electron oxidation event drives two proton transfers, this is known as a one-electron two-proton transfer (E2PT) process yielding 2’.20 By inserting a second benzimidazole, construct 3 was synthesized, allowing an E3PT

Figure 1. Cyclic voltammograms and experimental and calculated redox potentials. (A) Cyclic voltammograms of 1 (grey), 2 (blue), 3 (magenta) and 4 (green) in dry CH2Cl2. (B) Experimental and calculated E1/2 potentials for the redox couples indicated in Scheme 1. For each compound, the calculated, through-space distance (Å) between the phenol oxygen and the final proton acceptor nitrogen is indicated (blue wedge). Agreement between calculated and experimental values for 3 is by construction because this species was used as the reference for all species except 1, for which unsubstituted BIP was used as the reference (Table S2).

process to give 3’ as the product. Similarly, 4 was formed by inserting a third benzimidazole to provide a platform for an E4PT process and the formation of 4’, corresponding to proton translocation across ~16 Å. As indicated in Scheme 1, compounds 1–4 exhibit internal hydrogen bonds that provide well-defined structural frameworks required for transport of protons by a Grotthuss type mechanism.21 The presence of a strong hydrogen bond between the phenolic proton and the nitrogen lone pair of the adjacent benzimidazole in 1–4 has been established in related compounds.13-14, 20, 22 The intramolecular hydrogen bond between the benzimidazole NH and the terminal imine nitrogen in 2–4, and the hydrogen bonds connecting the benzimidazole moieties (for 3 and 4) are clearly indicated by 1H NMR chemical shifts at low field (SI, sections 2 and 3) and IR absorption features (vide infra).

base in the synthetic design. Further, density functional theory (DFT) calculations indicate that the hydrogen-bonded structure of 4 in Scheme 1 is the most thermodynamically stable of the extensive set of conformations examined (Figure S21). Figure 1A shows cyclic voltammograms of the phenoxyl radical/phenol couple recorded for compounds 1–4 (Table S1). We measured a 60 mV drop in the E1/2 following addition of each benzimidazole unit, indicating the phenol becomes easier to oxidize as successive benzimidazole groups are inserted. The computed redox potentials with all protons transferred for each species are within the accuracy of DFT calculations and indicate a decrease of 100 mV/benzimidazole across the series, which is consistent with the 60 mV observed (Figure 1B, colored dash lines and Table S2). Furthermore, theory quantifies the contributions of individual proton transfer reactions to the overall thermodynamics (Figure 1B, uncolored lines). In this model, all 2

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Journal of the American Chemical Society 50 mV increments to generate increasing amounts of the oxidized species. Black lines correspond to the neutral species, and the dotted line in D and H corresponds to the spectrum obtained upon polarizing the solution to reducing potentials after oxidizing for 2 min at a potential required to deplete 4. The upward arrows show the appearance of the characteristic band for either the benzimidazolium ion (1’) in A and E or the protonated imine (2’–4’) in F, G, and H. The band at 1670 cm-1, corresponding to the stretching mode of the amide carbonyl, shifts to 1678 cm-1 upon oxidation (see downward arrow in E).

proton transfers are found to be individually thermodynamically favorable upon oxidation of the phenol, even those between two benzimidazole units, which are the least thermodynamically favorable. The difference between the theoretical E1/2 for the phenoxyl radical/phenol couple (E0PT) and the E1/2 value for the 1’/1 couple (E1PT) is attributed to the initial proton transfer, from the phenoxyl radical cation to the proximal benzimidazole. It is the most thermodynamically downhill in each case and is quantified only by DFT because oxidation of phenols without appended bases is typically irreversible and therefore E1/2 is poorly defined.24 The final proton transfer yielding the protonated imine is less thermodynamically favorable, as expected given the lower ΔpKa for this step compared to that of the first step. In general, each proton transfer decreases the redox potential by the ΔpKa associated with that proton transfer (Table S2). Because all proton transfers are thermodynamically favorable upon oxidation, the phenol becomes easier to oxidize with additional proton transfers. This analysis of the elementary processes within a thermodynamic cycle is not intended to suggest a stepwise mechanism involving discreet intermediates for the EnPT process, but rather provides insight into the relative contribution of each proton transfer to the overall redox potential. The combined electrochemical and DFT data are consistent with an effectively concerted mechanism with no stable intermediates on the electrochemical timescale. Infrared spectroelectrochemical (IRSEC) measurements were carried out to examine the changes in the IR spectra of compounds 1–4 upon oxidation of the phenol and to identify the site of protonation (Figure 2).

In the high-frequency region (3480–3200 cm-1, Figure 2B, C, D) of 2–4, the band at ~3370 cm-1 corresponds to the imidazole NH stretching and is sensitive to hydrogen bonding. For example, the imidazole NH stretching not involved in hydrogen bonding observed in unsubstituted BIP appears at 3414 cm-1.20 In the case of 2–4, the shift to lower wavenumbers indicates that the NH of the imidazoles is involved in hydrogen bonds. The similarity of the spectra before and after oxidation of the phenol implies that these hydrogen bond networks persist. Conservation of the hydrogen bond networks following oxidation and proton translocation is a precondition for a reversible process (vide infra). In 1, the strong broad band with a maximum at 3316 cm-1 (Figure 2A) corresponds to the formation of the benzimidazolium ion (1’, Scheme 1) signaling an E1PT process;20 the analogous band is absent in the IRSEC of 2–4. In the lower frequency region (Figure 2E), the appearance in 1 of the band at 1556 cm-1 is another indication of benzimidazolium ion formation, as expected for an E1PT process.20 The appearance of the band at 1660 cm-1 in 2–4 (Figure 2F, G, H) indicates protonation of the imine nitrogen and provides definitive evidence for proton translocation from the phenol to the imine via E2PT, E3PT and E4PT processes in 2, 3, and 4, respectively. The computed infrared spectra for compounds 2–4 clearly show the appearance of this band (Figure S20), which is attributed to the coupling between the C=N stretching and the C=N+–H bending modes;25 it has been found in the IRSEC of compounds related to 2.22 The absence of the band at ~1556 cm-1 in 2–4 indicates that the benzimidazolium ion is not detectable in these experiments and further corroborates the long-distance translocation of protons upon oxidation.13, 20 The reversible electrochemical oxidation of 4 is depicted in Figure 2D and H. It is remarkable that upon reduction of the phenoxyl radical a reversal of the four-proton translocation takes place and, within experimental error, complete recovery of the initial neutral species of 4 is observed. Similar reversibility is observed for 1–3 (Figure S18). The chemical reversibility of the phenoxyl radical/phenol couple, uncommon for simple phenols, is attributed to the ability of the proton to shuttle between acidic and basic sites comprising the hydrogen bond network via intramolecular processes. In summary, a series of four bioinspired, redox-driven, protontranslocating compounds have been designed and studied experimentally and theoretically. The results of the IRSEC experiments are definitive – the one-electron oxidation of the phenol moiety of 1–4 results in reversible ΔpKa driven proton rearrangements extending over ~3, ~7, ~11 and ~16 Å to the terminal proton acceptor in 1, 2, 3 and 4, respectively. DFT calculations of redox potentials predicated on concerted or nearly concerted PCET processes with all protons transferring as postulated predicted the experimental observations.7, 20 Combining theoretical guidance, experimental measurements, and new synthetic designs we should be able to tweak the relative

Figure 2. Infrared spectroelectrochemical (IRSEC) spectra of compounds 1–4 recorded in dry CH2Cl2. (A), (B), (C) and (D) are IRSEC in the high frequency region (3480–3200 cm-1) and (E), (F), (G) and (H) correspond to the low frequency region (1720–1490 cm-1). Colored lines correspond to the oxidized species (color coded as in Figure 1) following polarization in

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1. Blankenship, R. E., Molecular Mechanisms of Photosynthesis Second Edition ed.; Wiley Blackwell: Oxford, 2014. 2. Mitchell, P., Coupling of Phosphorylation to Electron and Hydrogen Transfer by a Chemi-Osmotic Type of Mechanism. Nature 1961, 191, 144-148. 3. Migliore, A.; Polizzi, N. F.; Therien, M. J.; Beratan, D. N., Biochemistry and Theory of Proton-Coupled Electron Transfer. Chem. Rev. 2014, 114, 3381-3465. 4. Reece, S. Y.; Nocera, D. G., Proton-Coupled Electron Transfer in Biology: Results from Synergistic Studies in Natural and Model Systems. Annu. Rev. Biochem. 2009, 78, 673-699. 5. Stubbe, J.; Nocera, D. G.; Yee, C. S.; Chang, M. C., Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range ProtonCoupled Electron Transfer? Chem. Rev. 2003, 103, 2167-2201. 6. Dempsey, J. L.; Winkler, J. R.; Gray, H. B., Proton-Coupled Electron Flow in Protein Redox Machines. Chem. Rev. 2010, 110, 70247039. 7. Hammes-Schiffer, S.; Stuchebrukhov, A. A., Theory of Coupled Electron and Proton Transfer Reactions. Chem. Rev. 2010, 110, 6939-6960. 8. Zhong, D., Electron Transfer Mechanisms of DNA Repair by Photolyase. Annu. Rev. Phys. Chem. 2015, 66, 691-715. 9. Mathes, T.; van Stokkum, I. H.; Stierl, M.; Kennis, J. T., Redox Modulation of Flavin and Tyrosine Determines Photoinduced ProtonCoupled Electron Transfer and Photoactivation of Bluf Photoreceptors. J. Biol. Chem. 2012, 287, 31725-31738. 10. Tommos, C.; Babcock, G. T., Proton and Hydrogen Currents in Photosynthetic Water Oxidation. Biochim. Biophys. Acta, Bioenerg. 2000, 1458, 199-219. 11. Umena, Y.; Kawakami, K.; Shen, J. R.; Kamiya, N., Crystal Structure of Oxygen-Evolving Photosystem II at a Resolution of 1.9 Å. Nature 2011, 473, 55-60. 12. Guo, Z.; He, J.; Barry, B. A., Calcium, Conformational Selection, and Redox-Active Tyrosine Yz in the Photosynthetic Oxygen-Evolving Cluster. Proc. Natl. Acad. Sci. USA 2018, 115, 5658-5663. 13. Mora, S. J.; Odella, E.; Moore, G. F.; Gust, D.; Moore, T. A.; Moore, A. L., Proton-Coupled Electron Transfer in Artificial Photosynthetic Systems. Acc. Chem. Res. 2018, 51, 445-453. 14. Markle, T. F.; Rhile, I. J.; DiPasquale, A. G.; Mayer, J. M., Probing Concerted Proton-Electron Transfer in Phenol-Imidazoles. Proc. Natl. Acad. Sci. USA 2008, 105, 8185-8190. 15. Benisvy, L.; Bittl, R.; Bothe, E.; Garner, C. D.; McMaster, J.; Ross, S.; Teutloff, C.; Neese, F., Phenoxyl Radicals Hydrogen-Bonded to Imidazolium: Analogues of Tyrosyl D of Photosystem II: High-Field EPR and DFT Studies. Angew. Chem., Int. Ed. Engl. 2005, 44, 5314-5317. 16. Chararalambidis, G.; Das, S.; Trapali, A.; Quaranta, A.; Orio, M.; Halime, Z.; Fertey, P.; Guillot, R.; Coutsolelos, A.; Leibl, W.; Aukauloo, A.; Sircoglou, M., Water Molecules Gating a Photoinduced One-Electron TwoProtons Transfer in a Tyrosine/Histidine (Tyr/His) Model of Photosystem II. Angew. Chem., Int. Ed. Engl. 2018, 57, 9013-9017. 17. Megiatto, J. D., Jr.; Mendez-Hernandez, D. D.; Tejeda-Ferrari, M. E.; Teillout, A. L.; Llansola-Portoles, M. J.; Kodis, G.; Poluektov, O. G.; Rajh, T.; Mujica, V.; Groy, T. L.; Gust, D.; Moore, T. A.; Moore, A. L., A Bioinspired Redox Relay that Mimics Radical Interactions of the Tyr-His Pairs of Photosystem II. Nat. Chem. 2014, 6, 423-428. 18. Bonin, J.; Costentin, C.; Robert, M.; Savéant, J.-M.; Cedric, T., Hydrogen-Bond Relays in Concerted Proton Electron Transfers. Acc. Chem. Res. 2012, 45, 372-381. 19. Chrysina, M.; de Mendonça Silva, J. C.; Zahariou, G.; Pantazis, D. A.; Ioannidis, N., Proton Translocation Via Tautomerization of Asn298 During the S2–S3 State Transition in the Oxygen-Evolving Complex of Photosystem II. J. Phys. Chem. B 2019, 123, 3068-3078. 20. Huynh, M. T.; Mora, S. J.; Villalba, M.; Tejeda-Ferrari, M. E.; Liddell, P. A.; Cherry, B. R.; Teillout, A.-L.; Machan, C. W.; Kubiak, C. P.; Gust, D.; Moore, T. A.; Hammes-Schiffer, S.; Moore, A. L., Concerted OneElectron Two-Proton Transfer Processes in Models Inspired by the Tyr-His Couple of Photosystem II. ACS Cent. Sci. 2017, 3, 372-380. 21. Agmon, N., The Grotthuss Mechanism. Chem. Phys. Lett. 1995, 244, 456-462.

pKa’s of intervening proton relays so that the cost in redox potential of long-distance proton transfer can be better defined and controlled. Understanding the parameters controlling reversible proton transfer over an extended hydrogen bond network such as those described herein foretells the development of artificial bioinspired energy coupling membranes capable of the full range of reversible bioenergetic processes observed in nature.

ASSOCIATED CONTENT Supporting Information Experimental: materials and methods, synthesis and structural characterization, NMR data, electrochemical measurements, IRSEC, and IR data. Computational: details of electronic structure calculations, calculation of redox potentials, analysis of the thermodynamics of PCET reactions, computed IRSEC spectra and band assignments, and optimized cartesian coordinates of species studied. Additional references. This material is available free of charge via the Internet at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author * E-mail: [email protected] * E-mail: [email protected] * E-mail: [email protected]

ORCID Emmanuel Odella: 0000-0002-7021-400X Brian L. Wadsworth: 0000-0002-0274-9993 S. Jimena Mora: 0000-0003-4181-4732 Joshua J. Goings: 0000-0002-2817-1966 Mioy T. Huynh: 0000-0002-0472-7624 Devens Gust: 0000-0003-0550-8498 Thomas A. Moore: 0000-0002-1577-7117 Gary F. Moore: 0000-0003-3369-9308 Sharon Hammes-Schiffer: 0000-0002-3782-6995 Ana L. Moore: 0000-0002-6653-9506

Author Contributions ‡ These authors contributed equally.

Notes The authors declare no competing financial interests.

ACKNOWLEDGMENT This research was supported by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Award DEFG02-03ER15393. The theoretical portion of this research was supported as part of the Center for Molecular Electrocatalysis, an Energy Frontier Research Center, funded by the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences.

REFERENCES 4

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Journal of the American Chemical Society 22. Odella, E.; Mora, S. J.; Wadsworth, B. L.; Huynh, M. T.; Goings, J. J.; Liddell, P. A.; Groy, T. L.; Gervaldo, M.; Sereno, L. E.; Gust, D.; Moore, T. A.; Moore, G. F.; Hammes-Schiffer, S.; Moore, A. L., Controlling ProtonCoupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays. J. Am. Chem. Soc. 2018, 140, 15450-15460. 23. Forés, M.; Duran, M.; Solà, M.; Orozco, M.; Luque, F. J., Theoretical Evaluation of Solvent Effects on the Conformational and Tautomeric Equilibria of 2-(2‘-Hydroxyphenyl)Benzimidazole and on its Absorption and Fluorescence Spectra. J. Phys. Chem. A 1999, 103, 45254532.

24. Richards, J. A.; Whitson, P. E.; Evans, D. H., Electrochemical Oxidation of 2,4,6-Tri-Tert-Butylphenol. J. Electroanal. Chem. Interfacial Electrochem. 1975, 63, 311-327. 25. Lopez-Garriga, J. J.; Babcock, G. T.; Harrison, J. F., Factors Influencing the C=N Stretching Frequency in Neutral and Protonated Schiff's Bases. J. Am. Chem. Soc. 1986, 108, 7241-7251.

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1.04

~3

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~7

0.76

~11

0.70

~16

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Proton translocation distance (Å)

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E1/2 (V vs SCE)

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