Proton-Coupled Electron Transfer in Artificial Photosynthetic Systems

Jan 8, 2018 - Biography. S. Jimena Mora received her Ph.D. from the National University of Río Cuarto, Argentina. She is a postdoctoral associate at ...
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Article Cite This: Acc. Chem. Res. 2018, 51, 445−453

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Proton-Coupled Electron Transfer in Artificial Photosynthetic Systems S. Jimena Mora, Emmanuel Odella, Gary F. Moore, Devens Gust,* Thomas A. Moore,* and Ana L. Moore* School of Molecular Sciences, Arizona State University, Tempe, Arizona 85287, United States

CONSPECTUS: Artificial photosynthetic constructs can in principle operate more efficiently than natural photosynthesis because they can be rationally designed to optimize solar energy conversion for meeting human demands rather than the multiple needs of an organism competing for growth and reproduction in a complex ecosystem. The artificial photosynthetic constructs described in this Account consist primarily of covalently linked synthetic chromophores, electron donors and acceptors, and proton donors and acceptors that carry out the light absorption, electron transfer, and proton-coupled electron transfer (PCET) processes characteristic of photosynthetic cells. PCET is the movement of an electron from one site to another accompanied by proton transfer. PCET and the transport of protons over tens of angstroms are important in all living cells because they are a fundamental link between redox processes and the establishment of transmembrane gradients of proton electrochemical potential, known as proton-motive force (PMF), which is the unifying concept in bioenergetics. We have chosen a benzimidazole phenol (BIP) system as a platform for the study of PCET because with appropriate substitutions it is possible to design assemblies in which one or multiple proton transfers can accompany oxidation of the phenol. In BIP, oxidation of the phenol increases its acidity by more than ten pKa units; thus, electrochemical oxidation of the phenol is associated with a proton transfer to the imidazole. This is an example of a PCET process involving transfer of one electron and one proton, known as electron−proton transfer (EPT). When the benzimidazole moiety of BIP is substituted at the 4-position with good proton acceptor groups such as aliphatic amines, experimental and theoretical results indicate that two proton transfers occur upon one-electron oxidation of the phenol. This phenomenon is described as a one-electron−two-proton transfer (E2PT) process and results in translocation of protons over ∼7 Å via a Grotthuss-type mechanism, where the protons traverse a network of internally H-bonded sites. In the case of the E2TP process involving BIP analogues with amino group substituents, the thermodynamic price paid in redox potential to move a proton to the final proton acceptor is ∼300 mV. In this example, the decrease in redox potential limits the oxidizing power of the resulting phenoxyl radical. Thus, unlike the biological counterpart, the artificial construct is thermodynamically incapable of effectively advancing the redox state of a water oxidation catalyst. The design of systems where multiple proton transfer events are coupled to an oxidation reaction while a relatively high redox potential is maintained remains an outstanding challenge. The ability to control proton transfer and activity at defined distances and times is key to achieving proton management in the vicinity of catalysts operating at low overpotential in myriad biochemically important processes. Artificial photosynthetic constructs with welldefined structures, such as the ones described in this Account, can provide the means for discovering design principles upon which efficient redox catalysts for electrolysis and fuel cells can be based. the reaction-center excited state (P680*) reduces a nearby chlorophyll (Chl), forming P680•+ and Chl•−; this charge separation is the

I. INTRODUCTION In photosystem II (PSII), tyrosine Z (Tyrz) serves as a highpotential electron transfer mediator between the reaction-center chlorophylls (P680) and the oxygen-evolving complex (OEC), where water oxidation occurs (Figure 1).1,2 Upon illumination, © 2018 American Chemical Society

Received: October 1, 2017 Published: January 8, 2018 445

DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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Accounts of Chemical Research

Figure 1. (A) Partial structure of the PSII reaction center showing the cofactors involved in the photoinduced multistep electron transfer process. The lines between the cofactors show the distances in Å (red). (B) H-bond network around the Tyrz−His190 residues, water molecules are shown by small red spheres (Protein Data Bank code 2WU23).

linked to the IrO2 nanoparticles, and this ensemble was attached to the semiconductor. The BIP-modified photoanode improved the cell performance by more than a factor of 2.15 Encouraged by this result, we have investigated the details of PCET involving BIP and its derivatives in which one or two proton transfer steps are coupled to a single electron transfer. This is the beginning of an effort to discover fundamental structural and thermodynamic factors involved in coupling of redox processes to proton transfer reactions and ultimately proton currents. Protons and redox-linked proton currents are central to bioenergetics and will likely play an important role in the rational design of artificial and reengineered photosynthesis with improved energy conversion efficiency.16

light-driven electron transfer reaction of water oxidation. Subsequent electron transfers result in a reduced quinone and proton uptake on the stromal side of the thylakoid membrane. P680•+ participates in water oxidation and proton release by oxidizing Tyrz, which lies near the thylakoid lumen.3−5 During oxidation, Tyrz donates the proton to its H-bonded partner, a histidine residue (His190), yielding a neutral radical (Tyrz•) H-bonded to HisH+190. The thermodynamic activity of this proton, which is determined by the pKa of the residues and the protein matrix, is key to maintaining the high potential associated with the Tyrz•/Tyrz redox couple. Model studies indicate that if the phenolic proton associated with the Tyrz−His190 pair were lost to the surroundings, the potential of the resulting Tyrz•/Tyr− couple would be too low to oxidize water, and if the proton were not transferred to His190, the oxidation and formation of TyrzH•+ by P680•+ would be thermodynamically unfavorable. This apparent paradox that the Tyrz• radical must form and yet must conserve much of the potential of P680•+ in order to oxidize the OEC can be resolved by applying the concept of proton-coupled electron transfer (PCET), wherein the redox reaction is accompanied by proton transfer to His190 and the proton is constrained in the H-bond with Tyrz•.6 Moreover, the activity of the shared proton in Tyrz•−HisH+190 plays a role in the rapid reduction of P680•+, thereby ensuring the high quantum yield of the electron transfer processes between P680•+ and the OEC during advancement of the Kok cycle.2 Because of its central role in photosynthetic water oxidation, this PCET process has been widely studied.7 A significant number of model systems inspired by the function of the Tyrz−His190 pair in PSII have been developed.8−13 In collaboration with the group of T. E. Mallouk, we developed a dyesensitized photoelectrochemical cell that accomplished overall water splitting.14 The relatively low quantum yield of the original cell (∼1%) is due in part to kinetic competition between the productive forward reaction, oxidation of the catalyst for water oxidation (IrO2) by the photoxidized sensitizer (∼2.2 ms), and the unproductive recombination reaction, back electron transfer from the semiconductor (TiO2) to the oxidized sensitizer (∼0.37 ms). Inspired by the role of PCET in nature, we reasoned that the use of a redox mediator, a mimic of Tyrz−His190, would accelerate the reduction of the oxidized sensitizer by the catalyst. An additional electron transfer step, coupled with tight control of the proton activity, would more effectively compete with recombination and thereby improve the water splitting performance. A benzimidazole phenol (BIP; see 3 below) modified with a malonate group was

II. STRUCTURAL DESIGN The structures of two benzimidazole porphyrin dyads (1 and 2) that model the Tyrz−P680 components of the PSII reaction center are shown in Figure 2. In these compounds, high-potential porphyrins bearing two pentafluorophenyl groups (PF10) are models for P680 (redox potential ∼1.3 V vs NHE). The phenols model Tyrz and the benzimidazoles model its H-bonded partner, His190 (Figure 1).3 In 1, the benzimidazole moiety is the bridge between the porphyrin and the phenol, while in 2 the phenol is closer to the porphyrin and the spatial relationships are more reminiscent of those of His190, Tyrz, and P680. The H-bond between the phenolic OH and the lone pair of the proximal nitrogen of the benzimidazole in 2 is stronger than that in 1,10,11 as indicated by the chemical shift of the OH resonance in the 1H NMR spectra of 1 (13.5 ppm) and 2 (14.2 ppm) in dry chloroform. The larger chemical shift indicates a stronger H-bond.12,17 As a result of the enhanced electronic coupling between PF10 and the phenol in 2, the electron-withdrawing effect of PF10 is stronger, leading to a lower pKa of the phenol and a better match with the pKa of the benzimidazolium ion (the pKa’s of phenol and benzimidazolium ion in acetonitrile are 27 and 14, respectively).12,18 In the case of 1, the effect is opposite, lowering the pKa of the benzimidazolium ion. In general, similar pKa’s between partners of a H-bonded pair results in a stronger H-bond.12 The crystal structure of 2 shows an O···N distance of 2.58 Å, approaching that between the phenol oxygen of Tyrz and the imidazole nitrogen of His190 (2.4 Å).3,11 Triad systems were constructed by hydrolyzing the ester of 2 and using the resulting carboxylic acid as an anchor to attach the dyad to 446

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Figure 2. (A) Structure of benzimidazole phenol−porphyrin dyad 1. (B) Structure of benzimidazole phenol−porphyrin dyad 2. At the center, the crystal structure of 2 shows the distance of 2.58 Å between the phenol oxygen and the imidazole nitrogen, and the dihedral angle of 14.6° between the phenol and the benzimidazole groups is shown at the right (the tert-butyl group ortho to the phenol has been deleted for clarity).11

Figure 3. Triad system consisting of 2 attached to a SnO2 nanoparticle. Steps 1, 2, and 3 are described in the text.

TiO2 or SnO2 nanoparticle electron acceptors (see Figure 3).11,19 A triad was also formed using a tetracyanoporphyrin as a molecular electron acceptor attached to a modified version of 2 via an amide linkage.20 These triads were prepared to investigate PCET processes that result in the formation of distonic radical cations in which, following a photoinitiated multistep electron transfer process, an unpaired electron and charge are present in different regions of the molecule. As depicted in Figure 3, upon excitation of PF10 (step 1), an electron is injected into the conduction band of SnO2, generating PF10•+ (step 2). Secondary electron transfer from the phenol to PF10•+ is accompanied by proton transfer to the proximal nitrogen of the pendent benzimidazole and is driven by the reduction of the pKa of the phenol by more than ten pKa units as a consequence of the oxidation (step 3).6 The overall process generates a long-lived (∼93 μs) charge-separated state with the negative charge on the semiconductor and the positive charge on the benzimidazolium ion. The spin in the organic portion of the construct is concentrated mostly on the oxygen of the phenoxyl radical, with some delocalization into the macrocycle (vide infra). In the case of the triad containing a tetracyanoporphyrin in place of the SnO2 nanoparticle, the lifetime of the final charge-separated state is 9 μs.20 These are rather long lifetimes compared with those observed in other triad systems lacking a PCET step.21,22 Thus, the inclusion of a PCET step in multistep electron transfer processes is

one strategy for achieving high-energy, long-lived charge-separated states, which can be kinetically competent in subsequent redox processes.

III. CHARACTERIZATION OF THE PHENOXYL RADICAL AND ASSOCIATED BENZIMIDAZOLIUM ION Evidence for the formation of the phenoxyl radical following the photoinitiated electron transfer shown in Figure 3 comes from the appearance of new bands at ∼400 and ∼780 nm in the transient absorption spectrum, which are indicative of this species.19 Similar features are observed in spectroelectrochemical measurements of 3 (see Figure 4A).10,20 The chemical reversibility of the phenoxyl/phenol couple of 3 (Figure 4B, blue line) is attributed to the ability of the proton to shuttle between the oxygen and nitrogen lone-pair sites of the phenol−benzimidazole pair with minimal nuclear motion during the conversion between the reduced and oxidized forms. This short, highly restricted reaction coordinate traps the proton at the site of electrochemical activity. In the case of 4 (Figure 4B, red line), in which the internal H-bond and concomitant restricted reaction coordinate are not available, oxidation is coupled to loss of the phenolic proton, presumably to the bulk solution, resulting in a chemically irreversible redox process. 447

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interpreted as due primarily to solvation changes around the initial O−H···N site upon PCET.11 The gx values measured for this system are considerably smaller than the values observed for tyrosyl or phenoxyl radicals involved in H-bonds. This fact can be explained by the delocalization of the spin into the macrocycle.11,18 On the other hand, the gx value for a protonated phenoxyl radical in a BIP model compound has been estimated by density functional theory (DFT) to be as low as 2.004.26 The larger values of gx measured for illuminated samples of 2 attached to TiO2 (2.0056/2.0061) indicate that the transfer of the phenolic proton to the imidazole upon oxidation takes place even at 13 K. Infrared spectroelectrochemistry (IRSEC) is useful for identifying specific bonding changes due to protonation/deprotonation during a PCET process. Figure 5A shows the IRSEC spectra of 3 at a potential of ∼1.0 V vs SCE in the region of 3550−3100 cm−1; protonation of the benzimidazole moiety upon oxidation of the phenol was detected by the decrease in the intensity of the bands at ∼3400 cm−1, which correspond to the NH stretching of the benzimidazole moiety, and the concurrent appearance of the band at ∼3300 cm−1, which corresponds to the NH stretching of the benzimidazolium ion.12,18 Similar changes were observed following protonation using gaseous HCl (Figure 5B). Figure 5C shows the IRSEC spectra of 3 in the 1650−1500 cm−1 region, also measured at a potential of 1.0 V vs SCE. Changes in absorbance are indicated by upward and downward arrows. Many of the changes match rather closely the changes observed in the IR spectrum of 3 following treatment with HCl(g) (see the bands at 1626, 1556, and 1526 cm−1; arrows in Figure 5D). For example, the intensity of the band at 1556 cm−1 increases following application of the potential in the IRSEC experiment (Figure 5C) or upon treatment with HCl(g) in the IR measurement (Figure 5D), while the band at ∼1526 cm−1 decreases in intensity in the IRSEC experiment (Figure 5C) and is not detected in the IR spectrum upon protonation (Figure 5D). The band at 1556 cm−1 includes an in-plane NH bending vibration in the benzimidazolium ion, while the band at 1526 cm−1 includes an in-plane NH bending mode of the neutral benzimidazole.18 These bands exhibit shifts to lower wavenumbers upon deuteration, supporting the assignment of bending modes including the exchangeable proton of the NH group. The close correlation between the IRSEC and IR data provides clear evidence that protonation of the benzimidazole moiety to form the benzimidazolium ion takes places upon oneelectron oxidation of the phenol to form the phenoxyl radical.

Figure 4. (A) Spectroelectrochemistry of 3. The blue trace corresponds to the difference in absorption between the oxidized and neutral forms of 3. The oxidized form of 3 was generated by poising the working electrode at 1.05 V vs SCE. Solvent dichloroethane, 0.1 M tetrabutylammonium hexafluorophosphate (TBAPF6) as the supporting electrolyte.20 (B) Cyclic voltammograms of 3 (blue) and 4, an isomer of 3 (red). Solvent dichloromethane, 0.1 M TBAPF6, scan rate = 100 mV/s.6

Electron paramagnetic resonance (EPR) spectroscopy also provides clear spectroscopic evidence for the formation of the phenoxyl radical.10,11,23 Low-temperature illumination (using wavelengths greater than 520 nm at 4.2 K) of samples of 1 or 2 immobilized on TiO2 nanoparticles gives rise to signals in the X-band (9.5 GHz) EPR spectrum at fields of 3336−3450 G. The signals in this region are associated with unpaired electrons in the TiO2•− lattice. In addition to these features, signals from unpaired electrons in the organic part of the construct are observed at fields of 3270−3336 G. The radical residing in the organic component of the assembly was further studied using high-resolution D-band (130 GHz) EPR spectroscopy. The spectrum of 2 attached to TiO2 upon excitation with a 532 nm laser at 13 K is dominated by wellresolved anisotropic coupling tensors (gx = 2.0056; gy = 2.0042; gz = 2.0021). These values are in good agreement with those previously reported for tyrosyl radical of PSII.23 Theoretical and experimental EPR data from proteins and model compounds indicate that gx values for noninteracting tyrosyl or phenoxyl radicals in nonpolar environments are greater than 2.0080, while tyrosyl or phenoxyl radicals involved in H-bonds display gx values ranging from 2.0064 to 2.0075.24,25 After excitation and radical formation at 13 K in 2 attached to TiO2, the sample was annealed in the dark at 100 K for 10 min and then returned to 13 K, where a significant increase in the gx value from 2.0056 to 2.0061 was observed. The other two g tensor components remained unchanged. This shift is reminiscent of the temperature effects observed in the natural system23 and has been

IV. EXTENDING THE H-BOND NETWORK AROUND THE PHENOL In PSII, several putative proton channels consisting of H-bond networks involving amino acids and water molecules have been described.27,28 Some of them extend from the OEC to the thylakoid lumen,3 and proton transport could take place by a Grotthuss-type mechanism.29 Which ones are actively involved in transporting protons to the lumen remains an active area of research. It is certain that protons generated by water oxidation contribute to the generation of PMF30,31 and that P680•+ pays the price in redox potential to pump them into the lumen at high proton chemical potential. In the 1.9 Å resolution crystal structure of PSII, one of these proton channels, involving Tyrz, has been resolved.3 As shown in Figure 1B, Tyrz forms a strong H-bond with His190D1. This histidine in turn forms a H-bond to asparagine (Asn298D1), which also forms a strong H-bond to a water molecule. We modeled part of this H-bond network by functionalizing BIP (structure 7 in Figure 6).18 The functionalization at the 4-position of benzimidazole 448

DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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Accounts of Chemical Research

Figure 5. (A, C) Time courses of the IRSEC spectra of 3 at a potential of 1.0 V vs SCE in the 3550−3100 and 1650−1500 cm−1 regions, respectively. The structure below shows the radical cation formed by oxidation of 3. (B, D) IR spectra of 3 (black) and 3 protonated by treatment with excess HCl(g) (blue) in the 3550−3100 and 1650−1500 cm−1 regions, respectively. The structure below corresponds to protonated 3. Solvent dichloromethane, 0.1 M TBAPF6.18

transfer takes place in the natural system has not been confirmed, but if it does, it could be due to effects of the protein matrix, which can greatly affect the pKa’s of residues embedded within it. To carry out the second proton transfer, a better proton acceptor than the amide is required. Compounds 9 and 10 were synthesized for that purpose by reduction of 7 and 8 with lithium aluminum hydride.18

V. EVIDENCE FOR CONCERTED ONE-ELECTRON−TWO-PROTON TRANSFER Figure 7 depicts the one-electron−two-proton transfer (E2PT) process that could occur when 10 is oxidized. Theoretical and

Figure 6. Structures of benzimidazole phenol derivatives substituted at the 4-position and structure 7 showing the internal H-bonds.

began with the synthesis of 6 from methyl 2,3-diaminobenzoate and the substituted salicylaldehyde.10,20 Amide 7 was prepared by aminolysis of 6, and amide 8 was obtained by coupling of 5 and diethylamine with 1-(3-dimethylaminopropyl)-3-ethylcarbodiimide hydrochloride.18 The primary purpose for extending the H-bond network surrounding the phenol was to design a system where multiple proton transfers can be triggered by oxidation of the phenol. If this can be realized, transport of a proton at distances of 7 Å or more can be studied and the theory, thermodynamics and kinetics of multiple proton transfers coupled to a single oxidation explored. Compounds 7 and 8 model the Tyrz−His−Asn H-bond network of PSII (Figure 1B), and upon oxidation of the phenol, transfer of its proton to the proximal nitrogen of imidazole is expected, forming the benzimidazolium ion via an EPT process. However, for thermodynamic reasons the second proton transfer from the distal NH of the imidazolium ion to the carbonyl of the appended amide is disfavored (the pKa of the benzimidazolium ion is ∼14 and that of the protonated amide is ∼4 in acetonitrile).18 Whether such a proton

Figure 7. A 4-substituted BIP (10, BIP-CH2NEt2) that upon electrochemical oxidation of the phenol undergoes two proton transfers.

experimental studies clearly show that this transformation, which results in the formation of the phenoxyl radical and a protonated exocyclic tertiary amine, does occur. Below, some of the evidence for this mechanism is summarized. Electrochemical Studies

The redox potentials for compounds 5−10 were estimated by DFT calculations performed by M. T. Huynh in the group of 449

DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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Accounts of Chemical Research

On the other hand, because the potentials for the first oxidation of 9 and 10 are ∼300 mV lower than those of the other BIPs shown in Figure 6 (see Figure 8), the IRSEC spectrum of 10 shows substantial changes when the potential of 0.7 V vs SCE is applied. In the IR bond stretching region (3500−3000 cm−1), the initial benzimidazole NH band decreases and two new bands grow in. One of them, at 3460 cm−1, can be assigned to the proximal NH of the imidazole. Importantly, the formation of the benzimidazolium ion cannot be detected by the typical NH stretching band at ∼3300 cm−1 that is clearly seen in the spectra of 3 recorded at 1.0 V vs SCE (Figure 5A).18 Similarly, at lower wavenumbers (1575−1500 cm−1) no difference can be detected in the IRSEC spectra of 3 taken at 0.0 and 0.7 V vs SCE because the EPT process is expected to occur at ∼1.0 V vs SCE. In the same region, the IRSEC spectra of 10 at 0.7 V vs SCE has a band at 1529 cm−1 that increases in intensity, while the band at 1515 cm−1 decreases in intensity (Figure 9A). Importantly, no band grows in at 1556 cm−1 for 10, as was clearly observed for 3 after EPT. This band corresponds to the formation of the benzimidazolium ion and can be observed in the IR spectrum of 10 only after treatment with excess HCl(g), where both the exocyclic amino group and the benzimidazole moiety are expected to be protonated (Figure 9B). Thus, the EPT mechanism can be discarded in the case of 10.18 As mentioned above, the electrochemical data indicate that adding 2 equiv of TFA to a solution of 10 protonates the exocyclic amine and prevents the second proton transfer. Protonation of the exocyclic amine disrupts its H-bond with the distal NH of the benzimidazole. Upon addition of 2 equiv of TFA, the IR spectrum shows the disappearance of the band at 1515 cm−1 and the concomitant appearance of the band at 1529 cm−1 (Figure 9B). The band at 1515 cm−1 has a large component of the imidazole NH in-plane bending vibration, comparable to the band at 1526 cm−1 of 3 but at lower frequency. This is in agreement with the presence of an internal H-bond with the exocyclic amine. The band at 1529 cm−1 is characteristic of neutral benzimidazole NH bending. This band appears after the original H-bond between the NH of the imidazole and the exocyclic amine is disrupted. The fact that the IRSEC experiments (Figure 9A) show that the bands at 1515 and 1529 cm−1 change in the same way as they do following treatment with TFA (Figure 9B) suggests that protonation of the exocyclic amine and formation of a neutral imidazole accompany oxidation of the phenol. In summary, the IRSEC spectra of 10 at 0.7 V vs SCE supports the proton rearrangement of the E2PT mechanism depicted in Figure 7.18

S. Hammes-Schiffer and are in good agreement with experimental measurements.18,32 For all of the BIPs except 9 and 10, the calculated and experimental values for the first redox potentials are in the range of ∼0.9−1.0 V vs SCE in acetonitrile. Those values are associated with the concerted oxidation of the phenol and transfer of the phenolic proton to the benzimidazole in an EPT process. The DFT calculations predict that a concerted E2PT process would be thermodynamically possible in 9 and 10 and that a shift of the potentials by ∼300 mV to less positive values (∼0.6 V vs SCE) would be observed. As shown in the Supporting Information of ref 18, the DFT calculations for 10 indicate that this shift in midpoint potential can be associated with the ΔpKa between the benzimidazolium ion and the protonated tertiary amine. The ∼300 mV shift was confirmed experimentally (see Figure 8). We demonstrated

Figure 8. Cyclic voltammograms of compounds 6−10. Solvent acetonitrile, 0.5 M TBAPF6, scan rate = 100 mV/s.

that the observed redox waves at ∼0.6 vs SCE for 9 and 10 correspond to the oxidation of the phenol by comparing those values with the redox potentials of reference compounds lacking the phenol group, i.e., benzylamine and diethylbenzylamine. They exhibit irreversible oxidation waves at ∼1.5 and ∼0.9 V vs SCE, respectively.18 In another control experiment, a solution of 10 was titrated with trifluoracetic acid (TFA, pKa ∼ 13 in acetonitrile) to protonate the exocyclic amine (pKa ∼ 19 in acetonitrile) without protonating the benzimidazole group (pKa ∼ 14 in acetonitrile).18 When 2 equiv of TFA were added to the solution of 10, the initial oxidation wave at ∼0.6 V vs SCE disappeared and a new redox feature, similar to those associated with BIPs 3 and 5−8 (at ∼0.9−1.0 V vs SCE), was observed. We interpret this as good evidence for the E2PT process in 10 before protonation. After protonation of the exocyclic amine, the second proton transfer event is prevented, and thus, the wave at ∼0.6 V vs SCE typical of an E2PT process is replaced by one at ∼0.9 V vs SCE corresponding to the EPT process.18 At higher concentrations of TFA, oxidation of the protonated benzimidazole group is detected as a wave at ≥1.4 V vs SCE.6 Because the redox potential is reduced by ∼300 mV in 9 and 10, where the E2PT process is thermodynamically allowed, such species could not be used as relays in conjunction with wateroxidizing catalysts.15 The decrease in redox potential is certainly a function of the ΔpKa between the second proton donor and acceptor. Thus, for practical applications it will be important to find the minimum ΔpKa that will provide a sufficiently high redox potential to oxidize water at the desired rate.

Kinetic Isotope Effects

In general, measurable kinetic isotope effects (KIEs) are expected for PCET processes.7 However, there are examples where no KIEs have been detected, and theoretical explanations for such behavior have been offered.18,33,34 Table 1 presents experimental values obtained via electrochemical measurements performed on several of the compounds shown in Figure 6 as well as theoretical values obtained by assuming concerted PCET processes (EPT for 3 and 5−8, E2PT for 9 and 10).18 The theoretically predicted KIEs of ∼2.0 for compounds 5−8 are in reasonable agreement with the experimental values and in the range of experimental values obtained for related compounds in other laboratories.12,17,35−37 For 9 and 10, where two proton transfers are associated with oxidation of the phenol, the calculated KIE values and the experimental value for 10 are slightly smaller than those of 3 and 5−8. A theoretical explanation for the reduction in KIE is provided in the Supporting Information of ref 18.

Infrared Spectroelectrochemistry

The IRSEC spectrum of 3 at 0.7 V vs SCE does not show significant changes from the spectrum obtained at 0.0 V vs SCE. 450

DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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Figure 9. (A) Time course of the IRSEC spectra of 10 obtained at a potential of ∼0.7 V vs SCE. The structure below corresponds to the radical cation formed by oxidation of 10 via an E2PT process. (B) IR spectra of 10 in neutral form (black), 10 with the tertiary exocyclic amine protonated with 2 equiv of TFA (pink), and the product protonated with excess HCl(g) (blue). The structures below correspond to singly protonated (pink) and doubly protonated (blue) 10. Solvent dichloromethane, 0.1 M TBAPF6.

of specific vibrational modes in coupling electron and proton trajectories and the time scale and coherence of proton and electron motions in PCET processes. As mentioned above, proton transfers are central to bioenergetics, and managing proton activity in the vicinity of catalytic water oxidation and oxygen reduction sites is essential to efficient catalysis. Taking nature’s examples of water oxidation and respiration a step further, the generation of proton currents over lowresistance pathways to and from redox sites could be a step toward a reversible water electrolyzer/fuel cell constructthe technological equivalent of photosynthesis and respiration. These are key features of nature’s solar-based global ecosystem, which has a 3 billion year record of success. The challenge is to reimagine nature’s system as a solar-based industrial system supporting human activity so that further incursions on nature can be avoided.

Table 1. Calculated and Experimental Kinetic Isotope Effects

a b

compound

calculated KIE

3 − BIP 5 − BIP-COOH 6 − BIP-COOMe 7 − BIP-CONH2 8 − BIP-CONEt2 9 − BIP-CH2NH2 10 − BIP-CH2NEt2

1.9 2.0 2.1 1.8 2.0 1.6 1.3

a

experimental KIE 1.4b 1.5 ± 0.3 1.8 ± 0.3 1.7 ± 0.5 n/a n/a 0.9 ± 0.5

The uncertainties in the calculated KIEs are approximately ±0.5. Data for a related compound.36

Because of the relatively good agreement between the theoretical and experimental values for the KIE of 10, and in spite of the large error bar, we tentatively assign a concerted mechanism involving the transfer of two protons upon oxidation of the phenol (E2PT). However, a stepwise mechanism proceeding via an extremely shortlived intermediate cannot be discarded. Regardless of the mechanistic details, the process consists of a rearrangement of two protons in a H-bond network that extends over about 7 Å as a consequence of a one-electron oxidation event.

■

AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. *E-mail: [email protected]. *E-mail: [email protected]. ORCID

VII. CONCLUSIONS AND OUTLOOK In this Account, we have described the evolution of our work using constructs inspired by photosynthesis to find the structural and thermodynamic parameters required to couple proton transfer from a phenol to various benzimidazole derivatives upon oxidation of the phenol. In derivatives where the benzimidazole bears good proton acceptors, such as amines, we observed two proton transfers upon oxidation of the phenol (i.e., an E2PT process), which results in the translocation of protons over a distance of ca. 7 Å. This is a starting point for the design of bioinspired proton wires where proton transfer at longer distances (≫10 Å) can be envisioned. Although the oxidation of the phenol in the BIPs described here was electrochemically driven, the E2PT process could be lightdriven, for example, by substituting the BIP of photochemically activated triad systems with BIPs where E2PT processes are thermodynamically allowed. These constructs open the door to visible pump−IR probe and two-dimensional electronic spectroscopies that would address important mechanistic questions such as the role

Gary F. Moore: 0000-0003-3369-9308 Ana L. Moore: 0000-0002-6653-9506 Notes

The authors declare no competing financial interest. Biographies S. Jimena Mora received her Ph.D. from the National University of Río Cuarto, Argentina. She is a postdoctoral associate at Arizona State University. Emmanuel Odella received his Ph.D. from the National University of Río Cuarto, Argentina. He is a postdoctoral associate at Arizona State University. Gary F. Moore received his Ph.D. from Arizona State University, where he is now an assistant professor. Devens Gust received his Ph.D. from Princeton University. He is a Regents’ Professor Emeritus at Arizona State University. 451

DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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Accounts of Chemical Research

(15) Zhao, Y.; Swierk, J. R.; Megiatto, J. D., Jr.; Sherman, B.; Youngblood, W. J.; Qin, D.; Lentz, D. M.; Moore, A. L.; Moore, T. A.; Gust, D.; Mallouk, T. E. Improving the efficiency of water splitting in dye-sensitized solar cells by using a biomimetic electron transfer mediator. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15612−15616. (16) Ort, D. R.; Merchant, S. S.; Alric, J.; Barkan, A.; Blankenship, R. E.; Bock, R.; Croce, R.; Hanson, M. R.; Hibberd, J. M.; Long, S. P.; Moore, T. A.; Moroney, J.; Niyogi, K. K.; Parry, M. A. J.; Peralta-Yahya, P. P.; Prince, R. C.; Redding, K. E.; Spalding, M. H.; van Wijk, K. J.; Vermaas, W. F. J.; von Caemmerer, S.; Weber, A. P. M.; Yeates, T. O.; Yuan, J. S.; Zhu, X. G. Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proc. Natl. Acad. Sci. U. S. A. 2015, 112, 8529− 8536. (17) Rhile, I. J.; Markle, T. F.; Nagao, H.; DiPasquale, A. G.; Lam, O. P.; Lockwood, M. A.; Rotter, K.; Mayer, J. M. Concerted proton− electron transfer in the oxidation of hydrogen-bonded phenols. J. Am. Chem. Soc. 2006, 128, 6075−6088. (18) 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 one-electron two-proton transfer processes in models inspired by the Tyr-His couple of photosystem II. ACS Cent. Sci. 2017, 3, 372−380. (19) Llansola-Portolés, M. J.; Palacios, R. E.; Kodis, G.; Megiatto, J. D., Jr.; Moore, A. L.; Moore, T. A.; Gust, D. One approach to artificial photosynthesis. EPA Newsl. 2013, 84, 98−105. (20) Megiatto, J. D., Jr.; Antoniuk-Pablant, A.; Sherman, B. D.; Kodis, G.; Gervaldo, M.; Moore, T. A.; Moore, A. L.; Gust, D. Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation. Proc. Natl. Acad. Sci. U. S. A. 2012, 109, 15578−15583. (21) Liddell, P. A.; Kuciauskas, D.; Sumida, J. P.; Nash, B.; Nguyen, D.; Moore, A. L.; Moore, T. A.; Gust, D. Photoinduced charge separation and charge recombination to a triplet state in a carotene-porphyrinfullerene triad. J. Am. Chem. Soc. 1997, 119, 1400−1405. (22) Gust, D.; Moore, T. A.; Moore, A. L. Mimicking photosynthetic solar energy transduction. Acc. Chem. Res. 2001, 34, 40−48. (23) Faller, P.; Goussias, C.; Rutherford, A. W.; Un, S. Resolving intermediates in biological proton-coupled electron transfer: a tyrosyl radical prior to proton movement. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 8732−8735. (24) Un, S.; Dorlet, P.; Rutherford, A. W. A high-field EPR tour of radicals in photosystems I and II. Appl. Magn. Reson. 2001, 21, 341−361. (25) Orio, M.; Jarjayes, O.; Baptiste, B.; Philouze, C.; Duboc, C.; Mathias, J.-L.; Benisvy, L.; Thomas, F. Geometric and electronic structures of phenoxyl radicals hydrogen bonded to neutral and cationic partners. Chem. - Eur. J. 2012, 18, 5416−5429. (26) 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. 2005, 44, 5314−5317. (27) Vogt, L.; Vinyard, D. J.; Khan, S.; Brudvig, G. W. Oxygen-evolving complex of photosystem II: an analysis of second-shell residues and hydrogen-bonding networks. Curr. Opin. Chem. Biol. 2015, 25, 152− 158. (28) Bondar, A.-N.; Dau, H. Extended protein/water H-bond networks in photosynthetic water oxidation. Biochim. Biophys. Acta, Bioenerg. 2012, 1817, 1177−1190. (29) Agmon, N. The Grötthuss mechanism. Chem. Phys. Lett. 1995, 244, 456−462. (30) Blankenship, R. E. Molecular Mechanisms of Photosynthesis, 2nd ed.; Wiley Blackwell: Oxford, U.K., 2014; pp 137−138. (31) SteinbergYfrach, G.; Liddell, P. A.; Hung, S. C.; Moore, A. L.; Gust, D.; Moore, T. A. Conversion of light energy to proton potential in liposomes by artificial photosynthetic reaction centres. Nature 1997, 385, 239−241. (32) Solis, B. H.; Hammes-Schiffer, S. Proton-coupled electron transfer in molecular electrocatalysis: theoretical methods and design principles. Inorg. Chem. 2014, 53, 6427−6443.

Thomas A. Moore received his Ph.D. from Texas Tech University. He is a Regents’ Professor at Arizona State University. Ana L. Moore received her Ph.D. from Texas Tech University. She is a Regents’ Professor at Arizona State University.

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ACKNOWLEDGMENTS This work was supported by the Division of Chemical Sciences, Geosciences, and Biosciences, Office of Basic Energy Sciences, U.S. Department of Energy, under Contract DE-FG02-03ER15393. We thank Dr. Michael Vaughn for help with Figure 1.

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DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453

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DOI: 10.1021/acs.accounts.7b00491 Acc. Chem. Res. 2018, 51, 445−453