Role of Intact Hydrogen-Bond Networks in Multiproton-Coupled Electron Transfer

Guerra, Walter D.; Odella, Emmanuel; Secor, Maxim; Goings, Joshua J.; Urrutia, María N.; Wadsworth, Brian L.; Gervaldo, Miguel; Sereno, Leónides E.; Moore, Thomas A.; Moore, Gary F.; Hammes-Schiffer, Sharon; Moore, Ana L.

doi:10.1021/jacs.0c10474

Role of Intact Hydrogen-Bond Networks in Multiproton-Coupled Electron Transfer

Journal Article · Fri Dec 18 00:00:00 EST 2020 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.0c10474· OSTI ID:1831459

^[1]; ^[2]; ^[3]; ^[3]; ^[2]; ^[2]; ^[4]; ^[4]; ^[2]; ^[2]; ^[3]; ^[2]

Arizona State Univ., Tempe, AZ (United States); Arizona State University
Arizona State Univ., Tempe, AZ (United States)
Yale Univ., New Haven, CT (United States)
Univ. Nacional de Río Cuarto, Córdoba (Argentina)

The essential role of a well-defined hydrogen-bond network in achieving chemically reversible multiproton translocations triggered by one-electron electrochemical oxidation/reduction is investigated by using pyridylbenzimidazole–phenol models. The two molecular architectures designed for these studies differ with respect to the position of the N atom on the pyridyl ring. In one of the structures, a hydrogen-bond network extends uninterrupted across the molecule from the phenol to the pyridyl group. Experimental and theoretical evidence indicates that an overall chemically reversible two-protoncoupled electron-transfer process (E2PT) takes place upon electrochemical oxidation of the phenol. This E2PT process yields the pyridinium cation and is observed regardless of the cyclic voltammogram scan rate. In contrast, when the hydrogen-bond network is disrupted, as seen in the isomer, at high scan rates (~1000 mV s^–1) a chemically reversible process is observed with an E_1/2 characteristic of a one-proton-coupled electron-transfer process (E1PT). At slow cyclic voltammetric scan rates (<1000 mV s^–1) oxidation of the phenol results in an overall chemically irreversible two-proton-coupled electron-transfer process in which the second proton-transfer step yields the pyridinium cation detected by infrared spectroelectrochemistry. In this case, we postulate an initial intramolecular proton-coupled electron-transfer step yielding the E1PT product followed by a slow, likely intermolecular chemical step involving a second proton transfer to give the E2PT product. Insights into the electrochemical behavior of these systems are provided by theoretical calculations of the electrostatic potentials and electric fields at the site of the transferring protons for the forward and reverse processes. Furthermore, this work addresses a fundamental design principle for constructing molecular wires where protons are translocated over varied distances by a Grotthuss-type mechanism.

View Accepted Manuscript (DOE)

Research Organization:: Arizona State Univ., Tempe, AZ (United States)

Sponsoring Organization:: USDOE Office of Science (SC); USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: FG02-03ER15393; SC0021186

OSTI ID:: 1831459

Alternate ID(s):: OSTI ID: 1832128

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 52 Vol. 142; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (48)

Phenoxyl Radicals Hydrogen-Bonded to Imidazolium: Analogues of Tyrosyl D. of Photosystem II: High-Field EPR and DFT Studies Benisvy, Laurent; Bittl, Robert; Bothe, Eberhard Angewandte Chemie International Edition, Vol. 44, Issue 33 https://doi.org/10.1002/anie.200501132	journal	August 2005
Water Molecules Gating a Photoinduced One-Electron Two-Protons Transfer in a Tyrosine/Histidine (Tyr/His) Model of Photosystem II Chararalambidis, Georgios; Das, Shyamal; Trapali, Adelais Angewandte Chemie International Edition, Vol. 57, Issue 29 https://doi.org/10.1002/anie.201804498	journal	June 2018
Strategies to Enhance the Photosensitization: Polymerization and the Donor–Acceptor Even–Odd Effect Liu, Shunjie; Zhang, Haoke; Li, Yuanyuan Angewandte Chemie International Edition, Vol. 57, Issue 46 https://doi.org/10.1002/anie.201810326	journal	November 2018
Photodriven Multi-electron Storage in Disubstituted Ru ^II Dppz Analogues Aslan, Joseph M.; Boston, David J.; MacDonnell, Frederick M. Chemistry - A European Journal, Vol. 21, Issue 48 https://doi.org/10.1002/chem.201502607	journal	October 2015
On the Basicity of Conjugated Nitrogen Heterocycles in Different Media: On the Basicity of Conjugated Nitrogen Heterocycles in Different Media Lõkov, Märt; Tshepelevitsh, Sofja; Heering, Agnes European Journal of Organic Chemistry, Vol. 2017, Issue 30 https://doi.org/10.1002/ejoc.201700749	journal	August 2017
The FT-IR spectra of pyridine and pyridine-d5 Wong, Koon N.; Colson, Steven D. Journal of Molecular Spectroscopy, Vol. 104, Issue 1 https://doi.org/10.1016/0022-2852(84)90250-9	journal	March 1984
Infrared spectra of pyridinium salts in solution—I. The region of middle frequencies Glazunov, V. P.; Odinokov, S. E. Spectrochimica Acta Part A: Molecular Spectroscopy, Vol. 38, Issue 4 https://doi.org/10.1016/0584-8539(82)80014-7	journal	January 1982
Infrared spectra of pyridinium salts in solution—II. Fermi resonance and structure of νNH bands Glazunov, V. P.; Odinokov, S. E. Spectrochimica Acta Part A: Molecular Spectroscopy, Vol. 38, Issue 4 https://doi.org/10.1016/0584-8539(82)80015-9	journal	January 1982
Infrared spectra of pyridinium salts in solution—III. Associations of pyridinium salts with bases Odinokov, S. E.; Mashkovsky, A. A.; Nabiullin, A. A. Spectrochimica Acta Part A: Molecular Spectroscopy, Vol. 39, Issue 12 https://doi.org/10.1016/0584-8539(83)80126-3	journal	January 1983
A potentiometric study of acid–base equilibria of substituted pyridines in acetonitrile Augustin-Nowacka, D.; Chmurzyñski, L. Analytica Chimica Acta, Vol. 381, Issue 2-3 https://doi.org/10.1016/S0003-2670(98)00771-5	journal	February 1999
Proton and hydrogen currents in photosynthetic water oxidation Tommos, Cecilia; Babcock, Gerald T. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1458, Issue 1 https://doi.org/10.1016/S0005-2728(00)00069-4	journal	May 2000
A new insight into the vibrational analysis of pyridine Ureña, F. Partal; Gómez, M. Fernández; González, J. J. López Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, Vol. 59, Issue 12 https://doi.org/10.1016/S1386-1425(03)00082-9	journal	October 2003
Phenol and para-substituted phenols electrochemical oxidation pathways Enache, Teodor Adrian; Oliveira-Brett, Ana Maria Journal of Electroanalytical Chemistry, Vol. 655, Issue 1 https://doi.org/10.1016/j.jelechem.2011.02.022	journal	May 2011
Proton-Coupled Electron Transfer in Artificial Photosynthetic Systems Mora, S. Jimena; Odella, Emmanuel; Moore, Gary F. Accounts of Chemical Research, Vol. 51, Issue 2 https://doi.org/10.1021/acs.accounts.7b00491	journal	January 2018
Molecular Design for Electron-Driven Double-Proton Transfer: A New Scenario for Excited-State Proton-Coupled Electron Transfer Ren, Guanghua; Meng, Qingchi; Zhao, Jinfeng The Journal of Physical Chemistry A, Vol. 122, Issue 47 https://doi.org/10.1021/acs.jpca.8b09264	journal	November 2018
Proton-Coupled Electron Transfer in a Series of Ruthenium-Linked Tyrosines with Internal Bases: Evaluation of a Tunneling Model for Experimental Temperature-Dependent Kinetics Markle, Todd F.; Zhang, Ming-Tian; Santoni, Marie-Pierre The Journal of Physical Chemistry B, Vol. 120, Issue 35 https://doi.org/10.1021/acs.jpcb.6b05885	journal	August 2016
Nonequilibrium Dynamics of Proton-Coupled Electron Transfer in Proton Wires: Concerted but Asynchronous Mechanisms Goings, Joshua J.; Hammes-Schiffer, Sharon ACS Central Science, Vol. 6, Issue 9 https://doi.org/10.1021/acscentsci.0c00756	journal	September 2020
Concerted One-Electron Two-Proton Transfer Processes in Models Inspired by the Tyr-His Couple of Photosystem II Huynh, Mioy T.; Mora, S. Jimena; Villalba, Matias ACS Central Science, Vol. 3, Issue 5 https://doi.org/10.1021/acscentsci.7b00125	journal	April 2017
Biochemistry and Theory of Proton-Coupled Electron Transfer Migliore, Agostino; Polizzi, Nicholas F.; Therien, Michael J. Chemical Reviews, Vol. 114, Issue 7 https://doi.org/10.1021/cr4006654	journal	January 2014
Chemical Redox Agents for Organometallic Chemistry Connelly, Neil G.; Geiger, William E. Chemical Reviews, Vol. 96, Issue 2 https://doi.org/10.1021/cr940053x	journal	January 1996
Excited-State Intramolecular Proton Transfer in 2-(2-Hydroxyphenyl)benzimidazole and -benzoxazole: Effect of Rotamerism and Hydrogen Bonding Das, Kaustuv; Sarkar, Nilmoni; Ghosh, Ajit Kumar The Journal of Physical Chemistry, Vol. 98, Issue 37 https://doi.org/10.1021/j100088a006	journal	September 1994
Construction of Persistent Phenoxyl Radical with Intramolecular Hydrogen Bonding Maki, Toshihide; Araki, Yoko; Ishida, Yukihiro Journal of the American Chemical Society, Vol. 123, Issue 14 https://doi.org/10.1021/ja002453+	journal	March 2001
Concerted Proton−Electron Transfer in the Oxidation of Hydrogen-Bonded Phenols Rhile, Ian J.; Markle, Todd F.; Nagao, Hirotaka Journal of the American Chemical Society, Vol. 128, Issue 18 https://doi.org/10.1021/ja054167+	journal	April 2006
Proton-Coupled Electron Transfer from Tyrosine: A Strong Rate Dependence on Intramolecular Proton Transfer Distance Zhang, Ming-Tian; Irebo, Tania; Johansson, Olof Journal of the American Chemical Society, Vol. 133, Issue 34 https://doi.org/10.1021/ja203483j	journal	August 2011
Evaluation of Hydrogen-Bond Acceptors for Redox-Switchable Resorcin[4]arene Cavitands Pochorovski, Igor; Milić, Jovana; Kolarski, Dušan Journal of the American Chemical Society, Vol. 136, Issue 10 https://doi.org/10.1021/ja411429b	journal	February 2014
Proton-Coupled Electron Transfer from Tyrosine in the Interior of a de novo Protein: Mechanisms and Primary Proton Acceptor Nilsen-Moe, Astrid; Reinhardt, Clorice R.; Glover, Starla D. Journal of the American Chemical Society, Vol. 142, Issue 26 https://doi.org/10.1021/jacs.0c04655	journal	June 2020
Proton-Coupled Electron Transfer in a Strongly Coupled Photosystem II-Inspired Chromophore–Imidazole–Phenol Complex: Stepwise Oxidation and Concerted Reduction Manbeck, Gerald F.; Fujita, Etsuko; Concepcion, Javier J. Journal of the American Chemical Society, Vol. 138, Issue 36 https://doi.org/10.1021/jacs.6b03506	journal	September 2016
Isolating the Effects of the Proton Tunneling Distance on Proton-Coupled Electron Transfer in a Series of Homologous Tyrosine-Base Model Compounds Glover, Starla D.; Parada, Giovanny A.; Markle, Todd F. Journal of the American Chemical Society, Vol. 139, Issue 5 https://doi.org/10.1021/jacs.6b12531	journal	January 2017
Controlling Proton-Coupled Electron Transfer in Bioinspired Artificial Photosynthetic Relays Odella, Emmanuel; Mora, S. Jimena; Wadsworth, Brian L. Journal of the American Chemical Society, Vol. 140, Issue 45 https://doi.org/10.1021/jacs.8b09724	journal	October 2018
Proton-Coupled Electron Transfer Drives Long-Range Proton Translocation in Bioinspired Systems Odella, Emmanuel; Wadsworth, Brian L.; Mora, S. Jimena Journal of the American Chemical Society, Vol. 141, Issue 36 https://doi.org/10.1021/jacs.9b06978	journal	August 2019
Chemistry of 1,2,5-thiadiazoles. III. [1,2,5]thiadiazolo[3,4-c][1,2,5]thiadiazole Komin, Andrew P.; Street, Robert W.; Carmack, Marvin The Journal of Organic Chemistry, Vol. 40, Issue 19 https://doi.org/10.1021/jo00907a009	journal	September 1975
Extension of the Self-Consistent Spectrophotometric Basicity Scale in Acetonitrile to a Full Span of 28 p K _a Units: Unification of Different Basicity Scales Kaljurand, Ivari; Kütt, Agnes; Sooväli, Lilli The Journal of Organic Chemistry, Vol. 70, Issue 3 https://doi.org/10.1021/jo048252w	journal	February 2005
Effects of Protonation State on a Tyrosine−Histidine Bioinspired Redox Mediator ^† Moore, Gary F.; Hambourger, Michael; Kodis, Gerdenis The Journal of Physical Chemistry B, Vol. 114, Issue 45 https://doi.org/10.1021/jp101592m	journal	November 2010
One-Electron Redox Potentials of Phenols in Aqueous Solution Li, Cang; Hoffman, Morton Z. The Journal of Physical Chemistry B, Vol. 103, Issue 32 https://doi.org/10.1021/jp983819w	journal	August 1999
Theoretical Evaluation of Solvent Effects on the Conformational and Tautomeric Equilibria of 2-(2‘-Hydroxyphenyl)benzimidazole and on Its Absorption and Fluorescence Spectra Forés, Marta; Duran, Miquel; Solà, Miquel The Journal of Physical Chemistry A, Vol. 103, Issue 23 https://doi.org/10.1021/jp984773+	journal	May 1999
Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å Umena, Yasufumi; Kawakami, Keisuke; Shen, Jian-Ren Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09913	journal	April 2011
A bioinspired redox relay that mimics radical interactions of the Tyr–His pairs of photosystem II Megiatto Jr, Jackson D.; Méndez-Hernández, Dalvin D.; Tejeda-Ferrari, Marely E. Nature Chemistry, Vol. 6, Issue 5 https://doi.org/10.1038/nchem.1862	journal	February 2014
Artificial photosynthesis: closing remarks Hammarström, Leif Faraday Discussions, Vol. 198 https://doi.org/10.1039/C7FD00133A	journal	January 2017
Recent advances in bioinspired proton-coupled electron transfer Pannwitz, Andrea; Wenger, Oliver S. Dalton Transactions, Vol. 48, Issue 18 https://doi.org/10.1039/C8DT04373F	journal	January 2019
Proton-coupled electron transfer across benzimidazole bridges in bioinspired proton wires Odella, Emmanuel; Mora, S. Jimena; Wadsworth, Brian L. Chemical Science, Vol. 11, Issue 15 https://doi.org/10.1039/C9SC06010C	journal	January 2020
Redox potentials along the redox-active low-barrier H-bonds in electron transfer pathways Saito, Keisuke; Mandal, Manoj; Ishikita, Hiroshi Physical Chemistry Chemical Physics, Vol. 22, Issue 44 https://doi.org/10.1039/D0CP04265J	journal	January 2020
The Vibrational Spectra of Pyridine and Pyridine‐ d ₅ Corrsin, Lester; Fax, B. J.; Lord, R. C. The Journal of Chemical Physics, Vol. 21, Issue 7 https://doi.org/10.1063/1.1699158	journal	July 1953
Probing concerted proton-electron transfer in phenol-imidazoles Markle, T. F.; Rhile, I. J.; DiPasquale, A. G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 24 https://doi.org/10.1073/pnas.0708967105	journal	January 2008
Improving the efficiency of water splitting in dye-sensitized solar cells by using a biomimetic electron transfer mediator Zhao, Y.; Swierk, J. R.; Megiatto, J. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 39 https://doi.org/10.1073/pnas.1118339109	journal	April 2012
Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation Megiatto, J. D.; Antoniuk-Pablant, A.; Sherman, B. D. Proceedings of the National Academy of Sciences, Vol. 109, Issue 39 https://doi.org/10.1073/pnas.1118348109	journal	May 2012
Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Barry, B. A.; Babcock, G. T. Proceedings of the National Academy of Sciences, Vol. 84, Issue 20 https://doi.org/10.1073/pnas.84.20.7099	journal	October 1987
Vibrational Spectra of Pyridinium Salts Cook, Denys Canadian Journal of Chemistry, Vol. 39, Issue 10 https://doi.org/10.1139/v61-271	journal	October 1961
Proton-Coupled Electron Transfer in Biology: Results from Synergistic Studies in Natural and Model Systems Reece, Steven Y.; Nocera, Daniel G. Annual Review of Biochemistry, Vol. 78, Issue 1 https://doi.org/10.1146/annurev.biochem.78.080207.092132	journal	June 2009

Similar Records

Design and synthesis of benzimidazole phenol-porphyrin dyads for the study of bioinspired photoinduced proton-coupled electron transfer

Journal Article · Wed Jan 15 19:00:00 EST 2020 · Journal of Porphyrins and Phthalocyanines · OSTI ID:1800067

Related Subjects

37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY
Aromatic compounds
Molecular structure
Pyridyl
Reaction mechanisms
Redox reactions

Role of Intact Hydrogen-Bond Networks in Multiproton-Coupled Electron Transfer

Citation Formats

References (48)

Similar Records

Related Subjects