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.

doi:10.1021/jacs.6b03506

Proton-Coupled Electron Transfer in a Strongly Coupled Photosystem II-Inspired Chromophore–Imidazole–Phenol Complex: Stepwise Oxidation and Concerted Reduction

Journal Article · Thu Aug 18 00:00:00 EDT 2016 · Journal of the American Chemical Society

DOI:https://doi.org/10.1021/jacs.6b03506· OSTI ID:1336211

Manbeck, Gerald F. ^[1]; Fujita, Etsuko ^[1]; Concepcion, Javier J. ^[1]

Brookhaven National Lab. (BNL), Upton, NY (United States). Chemistry Division

Proton-coupled electron-transfer (PCET) reactions were studied in acetonitrile for a Photosystem II (PSII) inspired [Ru(bpy)₂(phen-imidazole-Ph(OH)(^tBu)₂)]²⁺, in which Ru(III) generated by a flash-quench sequence oxidizes the appended phenol and the proton is transferred to the hydrogen bonded imidazole base. In contrast to related systems, the donor and acceptor are strongly coupled, as indicated by the shift in the Ru^III/IIcouple upon phenol oxidation, and intramolecular oxidation of the phenol by Ru(III) is energetically favorable by both stepwise or concerted pathways. The phenol oxidation occurs via a stepwise ET-PT mechanism with k_ET = 2.7 × 10⁷ s^₋1 and a kinetic isotope effect (KIE) of 0.99 ± 0.03. The electron transfer reaction was characterized as adiabatic with λ_DA = 1.16 eV and 280 < H_DA < 540 cm^₋1 consistent with strong electronic coupling and slow solvent dynamics. Reduction of the phenoxyl radical by the quencher radical was examined as the analogue of the redox reaction between the PSII tyrosyl radical and the oxygen evolving complex (OEC). In our PSII-inspired complex, the recombination reaction activation energy is < 2 kcal mol^₋1. In conclusion, the reaction is nonadiabatic (V_PCET ~ 22 cm^₋1 (H) and 49 cm^₋1 (D)), concerted, and exhibits an unexpected inverse KIE of 0.55 that is attributed to greater overlap of the reactant vibronic ground state with the OD vibronic states of the proton acceptor due to the smaller quantum spacing of the deuterium vibrational levels.

View Accepted Manuscript (DOE)

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)

OSTI ID:: 1336211

Report Number(s):: BNL--113231-2016-JA; KC0304030

Journal Information:: Journal of the American Chemical Society, Journal Name: Journal of the American Chemical Society Journal Issue: 36 Vol. 138; ISSN 0002-7863

Publisher:: American Chemical Society (ACS)Copyright Statement

Country of Publication:: United States

Language:: English

References (114)

A Biomimetic Model of the Electron Transfer between P680 and the TyrZ-His190 Pair of PSII Lachaud, Fabien; Quaranta, Annamaria; Pellegrin, Yann Angewandte Chemie International Edition, Vol. 44, Issue 10 https://doi.org/10.1002/anie.200461948	journal	February 2005
Concerted Proton–Electron Transfer in Pyridylphenols: The Importance of the Hydrogen Bond Markle, Todd F.; Mayer, James M. Angewandte Chemie International Edition, Vol. 47, Issue 4 https://doi.org/10.1002/anie.200702486	journal	January 2008
Influence of the Protonic State of an Imidazole-Containing Ligand on the Electrochemical and Photophysical Properties of a Ruthenium(II)–Polypyridine-Type Complex Quaranta, Annamaria; Lachaud, Fabien; Herrero, Christian Chemistry - A European Journal, Vol. 13, Issue 29 https://doi.org/10.1002/chem.200700185	journal	October 2007
Photosystem II: The machinery of photosynthetic water splitting Renger, Gernot; Renger, Thomas Photosynthesis Research, Vol. 98, Issue 1-3 https://doi.org/10.1007/s11120-008-9345-7	journal	October 2008
Solvent relaxation dynamics and electron transfer Bixon, M.; Jortner, Joshua Chemical Physics, Vol. 176, Issue 2-3 https://doi.org/10.1016/0301-0104(93)80255-8	journal	October 1993
Electron transfers in chemistry and biology Marcus, R. A.; Sutin, Norman Biochimica et Biophysica Acta (BBA) - Reviews on Bioenergetics, Vol. 811, Issue 3 https://doi.org/10.1016/0304-4173(85)90014-X	journal	August 1985
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
Mechanism of photosynthetic water oxidation: combining biophysical studies of photosystem II with inorganic model chemistry Vrettos, John S.; Limburg, Julian; Brudvig, Gary W. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1503, Issue 1-2 https://doi.org/10.1016/S0005-2728(00)00214-0	journal	January 2001
Electron paramagnetic resonance kinetic studies of the S states in spinach PSII membranes Reza Razeghifard, M.; Pace, Ronald J. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1322, Issue 2-3 https://doi.org/10.1016/S0005-2728(97)00069-8	journal	December 1997
Energy surfaces, reorganization energies, and coupling elements in electron transfer Brunschwig, Bruce S.; Sutin, Norman Coordination Chemistry Reviews, Vol. 187, Issue 1 https://doi.org/10.1016/S0010-8545(98)00255-0	journal	June 1999
pH dependence of charge transfer between tryptophan and tyrosine in dipeptides Reece, Steven Y.; Stubbe, JoAnne; Nocera, Daniel G. Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1706, Issue 3 https://doi.org/10.1016/j.bbabio.2004.11.011	journal	February 2005
Back-reactions, short-circuits, leaks and other energy wasteful reactions in biological electron transfer: Redox tuning to survive life in O ₂ Rutherford, A. William; Osyczka, Artur; Rappaport, Fabrice FEBS Letters, Vol. 586, Issue 5 https://doi.org/10.1016/j.febslet.2011.12.039	journal	January 2012
Janus-faced charge recombinations in photosystem II photoinhibition Vass, Imre; Cser, Krisztian Trends in Plant Science, Vol. 14, Issue 4 https://doi.org/10.1016/j.tplants.2009.01.009	journal	April 2009
Moving Protons and Electrons in Biomimetic Systems Warren, Jeffrey J.; Mayer, James M. Biochemistry, Vol. 54, Issue 10 https://doi.org/10.1021/acs.biochem.5b00025	journal	March 2015
Proton-Coupled Electron Transfer and a Tyrosine–Histidine Pair in a Photosystem II-Inspired β-Hairpin Maquette: Kinetics on the Picosecond Time Scale Pagba, Cynthia V.; McCaslin, Tyler G.; Chi, San-Hui The Journal of Physical Chemistry B, Vol. 120, Issue 7 https://doi.org/10.1021/acs.jpcb.6b00560	journal	February 2016
Exploring Autoionization and Photoinduced Proton-Coupled Electron Transfer Pathways of Phenol in Aqueous Solution Oliver, Thomas A. A.; Zhang, Yuyuan; Roy, Anirban The Journal of Physical Chemistry Letters, Vol. 6, Issue 20 https://doi.org/10.1021/acs.jpclett.5b01861	journal	September 2015
Hydrogen-Bond Relays in Concerted Proton–Electron Transfers Bonin, Julien; Costentin, Cyrille; Robert, Marc Accounts of Chemical Research, Vol. 45, Issue 3 https://doi.org/10.1021/ar200132f	journal	October 2011
Proton-Coupled Electron Transfer with Photoexcited Metal Complexes Wenger, Oliver S. Accounts of Chemical Research, Vol. 46, Issue 7 https://doi.org/10.1021/ar300289x	journal	February 2013
Theory of Proton-Coupled Electron Transfer in Energy Conversion Processes Hammes-Schiffer, Sharon Accounts of Chemical Research, Vol. 42, Issue 12 https://doi.org/10.1021/ar9001284	journal	December 2009
Mimicking Photosynthetic Solar Energy Transduction Gust, Devens; Moore, Thomas A.; Moore, Ana L. Accounts of Chemical Research, Vol. 34, Issue 1 https://doi.org/10.1021/ar9801301	journal	January 2001
Kinetics and Pathways of Charge Recombination in Photosystem II ^† Rappaport, Fabrice; Guergova-Kuras, Mariana; Nixon, Peter J. Biochemistry, Vol. 41, Issue 26 https://doi.org/10.1021/bi025725p	journal	July 2002
Use of 3-Aminotyrosine To Examine the Pathway Dependence of Radical Propagation in Escherichia coli Ribonucleotide Reductase Minnihan, Ellen C.; Seyedsayamdost, Mohammad R.; Stubbe, JoAnne Biochemistry, Vol. 48, Issue 51 https://doi.org/10.1021/bi901439w	journal	December 2009
Proton/Hydrogen Transfer Affects the S-State-Dependent Microsecond Phases of P680 ⁺ Reduction during Water Splitting Schilstra, Maria J.; Rappaport, Fabrice; Nugent, Jonathan H. A. Biochemistry, Vol. 37, Issue 11 https://doi.org/10.1021/bi9713815	journal	February 1998
Function of Tyrosine Z in Water Oxidation by Photosystem II: Electrostatical Promotor Instead of Hydrogen Abstractor ^† Ahlbrink, Ralf; Haumann, Michael; Cherepanov, Dmitry Biochemistry, Vol. 37, Issue 4 https://doi.org/10.1021/bi9719152	journal	January 1998
The Role of Hydrogen Bonds for the Multiphasic P680 ⁺ ^• Reduction by Y _Z in Photosystem II with Intact Oxyen Evolution Capacity. Analysis of Kinetic H/D Isotope Exchange Effects ^† Christen, G.; Renger, G. Biochemistry, Vol. 38, Issue 7 https://doi.org/10.1021/bi982188t	journal	February 1999
Role of D1-His190 in the Proton-Coupled Oxidation of Tyrosine Y _Z in Manganese-Depleted Photosystem II ^† Hays, Anna-Maria A.; Vassiliev, Ilya R.; Golbeck, John H. Biochemistry, Vol. 38, Issue 37 https://doi.org/10.1021/bi990716a	journal	September 1999
Radical Initiation in the Class I Ribonucleotide Reductase: Long-Range Proton-Coupled Electron Transfer? Stubbe, JoAnne; Nocera, Daniel G.; Yee, Cyril S. Chemical Reviews, Vol. 103, Issue 6 https://doi.org/10.1021/cr020421u	journal	June 2003
Update 1 of: Electrochemical Approach to the Mechanistic Study of Proton-Coupled Electron Transfer Costentin, Cyrille; Robert, Marc; Savéant, Jean-Michel Chemical Reviews, Vol. 110, Issue 12 https://doi.org/10.1021/cr100038y	journal	December 2010
Theory of Coupled Electron and Proton Transfer Reactions Hammes-Schiffer, Sharon; Stuchebrukhov, Alexei A. Chemical Reviews, Vol. 110, Issue 12 https://doi.org/10.1021/cr1001436	journal	December 2010
Proton-Coupled Electron Transfer Weinberg, David R.; Gagliardi, Christopher J.; Hull, Jonathan F. Chemical Reviews, Vol. 112, Issue 7 https://doi.org/10.1021/cr200177j	journal	April 2012
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
Manganese Cluster in Photosynthesis: Where Plants Oxidize Water to Dioxygen Yachandra, Vittal K.; Sauer, Kenneth; Klein, Melvin P. Chemical Reviews, Vol. 96, Issue 7 https://doi.org/10.1021/cr950052k	journal	January 1996
Quantum Mechanical Continuum Solvation Models Tomasi, Jacopo; Mennucci, Benedetta; Cammi, Roberto Chemical Reviews, Vol. 105, Issue 8 https://doi.org/10.1021/cr9904009	journal	August 2005
Photochemistry of MLCT excited states. Effect of nonchromophoric ligand variations on photophysical properties in the series cis-Ru(bpy)2L22+ Caspar, Jonathan V.; Meyer, Thomas J. Inorganic Chemistry, Vol. 22, Issue 17 https://doi.org/10.1021/ic00159a021	journal	August 1983
Chemical Approaches to Artificial Photosynthesis. 2 Alstrum-Acevedo, James H.; Brennaman, M. Kyle; Meyer, Thomas J. Inorganic Chemistry, Vol. 44, Issue 20 https://doi.org/10.1021/ic050904r	journal	October 2005
Synthesis of Phosphonic Acid Derivatized Bipyridine Ligands and Their Ruthenium Complexes Norris, Michael R.; Concepcion, Javier J.; Glasson, Christopher R. K. Inorganic Chemistry, Vol. 52, Issue 21 https://doi.org/10.1021/ic4014976	journal	October 2013
Ab Initio Calculation of Vibrational Absorption and Circular Dichroism Spectra Using Density Functional Force Fields Stephens, P. J.; Devlin, F. J.; Chabalowski, C. F. The Journal of Physical Chemistry, Vol. 98, Issue 45, p. 11623-11627 https://doi.org/10.1021/j100096a001	journal	November 1994
Measurement of the extinction coefficient of the methyl viologen cation radical and the efficiency of its formation by semiconductor photocatalysis Watanabe, Tadashi; Honda, Kenichi The Journal of Physical Chemistry, Vol. 86, Issue 14 https://doi.org/10.1021/j100211a014	journal	July 1982
Comparison of substituent effects on dissociation and conjugation of phenols with those of carboxylic acids in acetonitrile, N,N-dimethylformamide, and dimethyl sulfoxide Chantooni, M. K.; Kolthoff, I. M. The Journal of Physical Chemistry, Vol. 80, Issue 12 https://doi.org/10.1021/j100553a009	journal	June 1976
Electron ejection and electron capture by phenolic compounds Feitelson, J.; Hayon, E. The Journal of Physical Chemistry, Vol. 77, Issue 1 https://doi.org/10.1021/j100620a003	journal	January 1973
Substituent effects on the stabilities of phenoxyl radicals and the acidities of phenoxyl radical cations Bordwell, Frederick G.; Cheng, Jinpei Journal of the American Chemical Society, Vol. 113, Issue 5 https://doi.org/10.1021/ja00005a042	journal	February 1991
Electron-Transfer Reactions of Ruthenium Trisbipyridyl-Viologen Donor-Acceptor Molecules: Comparison of the Distance Dependence of Electron Transfer-Rates in the Normal and Marcus Inverted Regions Yonemoto, Edward H.; Saupe, Geoffrey B.; Schmehl, Russell H. Journal of the American Chemical Society, Vol. 116, Issue 11 https://doi.org/10.1021/ja00090a026	journal	June 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
Kinetics of reduction of eight viologens by dithionite ion Tsukahara, K.; Wilkins, R. G. Journal of the American Chemical Society, Vol. 107, Issue 9 https://doi.org/10.1021/ja00295a013	journal	May 1985
Laser flash spectroscopy of tris(2,2'-bipyridine)ruthenium(II) in solution Bensasson, R.; Salet, C.; Balzani, V. Journal of the American Chemical Society, Vol. 98, Issue 12 https://doi.org/10.1021/ja00428a064	journal	June 1976
Measurement of rates of electron transfer between tris(2,2'-bipyridine)ruthenium(3+) and tris(1,10-phenanthroline)iron(2+) ions and between tris(1,10-phenanthroline)ruthenium(3+) and tris(2,2'-bipyridine)ruthenium(2+) ions by differential excitation flash photolysis Young, Roger C.; Keene, F. Richard; Meyer, Thomas J. Journal of the American Chemical Society, Vol. 99, Issue 8 https://doi.org/10.1021/ja00450a011	journal	April 1977
Normal and Inverse Primary Kinetic Deuterium Isotope Effects for C−H Bond Reductive Elimination and Oxidative Addition Reactions of Molybdenocene and Tungstenocene Complexes: Evidence for Benzene σ-Complex Intermediates Churchill, David G.; Janak, Kevin E.; Wittenberg, Joshua S. Journal of the American Chemical Society, Vol. 125, Issue 5 https://doi.org/10.1021/ja027670k	journal	February 2003
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
Electron Transfer Reactions of Fluorotyrosyl Radicals Reece, Steven Y.; Seyedsayamdost, Mohammad R.; Stubbe, JoAnne Journal of the American Chemical Society, Vol. 128, Issue 42 https://doi.org/10.1021/ja0636688	journal	October 2006
Concerted Proton−Electron Transfer Reactions in Water. Are the Driving Force and Rate Constant Depending on pH When Water Acts as Proton Donor or Acceptor? Costentin, Cyrille; Robert, Marc; Savéant, Jean-Michel Journal of the American Chemical Society, Vol. 129, Issue 18 https://doi.org/10.1021/ja067950q	journal	May 2007
Excited-State Quenching by Proton-Coupled Electron Transfer Concepcion, Javier J.; Brennaman, M. Kyle; Deyton, Jeremy R. Journal of the American Chemical Society, Vol. 129, Issue 22 https://doi.org/10.1021/ja069049g	journal	June 2007
Adiabatic and Non-adiabatic Concerted Proton−Electron Transfers. Temperature Effects in the Oxidation of Intramolecularly Hydrogen-Bonded Phenols Costentin, Cyrille; Robert, Marc; Savéant, Jean-Michel Journal of the American Chemical Society, Vol. 129, Issue 32 https://doi.org/10.1021/ja071150d	journal	August 2007
Buffer-Assisted Proton-Coupled Electron Transfer in a Model Rhenium−Tyrosine Complex Ishikita, Hiroshi; Soudackov, Alexander V.; Hammes-Schiffer, Sharon Journal of the American Chemical Society, Vol. 129, Issue 36 https://doi.org/10.1021/ja072708k	journal	September 2007
Proton-Coupled Electron Transfer of Tyrosine Oxidation: Buffer Dependence and Parallel Mechanisms Irebo, Tania; Reece, Steven Y.; Sjödin, Martin Journal of the American Chemical Society, Vol. 129, Issue 50 https://doi.org/10.1021/ja073012u	journal	December 2007
PELDOR Spectroscopy with DOPA-β2 and NH ₂ Y-α2s: Distance Measurements between Residues Involved in the Radical Propagation Pathway of E. coli Ribonucleotide Reductase Seyedsayamdost, Mohammad R.; Chan, Clement T. Y.; Mugnaini, Veronica Journal of the American Chemical Society, Vol. 129, Issue 51 https://doi.org/10.1021/ja076459b	journal	December 2007
A Hot Oxidant, 3-NO ₂ Y ₁₂₂ Radical, Unmasks Conformational Gating in Ribonucleotide Reductase Yokoyama, Kenichi; Uhlin, Ulla; Stubbe, JoAnne Journal of the American Chemical Society, Vol. 132, Issue 43 https://doi.org/10.1021/ja1069344	journal	November 2010
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
Proton Coupled Electron Transfer and Redox-Active Tyrosine Z in the Photosynthetic Oxygen-Evolving Complex Keough, James M.; Jenson, David L.; Zuniga, Ashley N. Journal of the American Chemical Society, Vol. 133, Issue 29 https://doi.org/10.1021/ja2041139	journal	July 2011
Kinetic Effects of Increased Proton Transfer Distance on Proton-Coupled Oxidations of Phenol-Amines Markle, Todd F.; Rhile, Ian J.; Mayer, James M. Journal of the American Chemical Society, Vol. 133, Issue 43 https://doi.org/10.1021/ja2056853	journal	November 2011
Influence of Donor–Acceptor Distance Variation on Photoinduced Electron and Proton Transfer in Rhenium(I)–Phenol Dyads Kuss-Petermann, Martin; Wolf, Hilke; Stalke, Dietmar Journal of the American Chemical Society, Vol. 134, Issue 30 https://doi.org/10.1021/ja3053046	journal	July 2012
Spanning Four Mechanistic Regions of Intramolecular Proton-Coupled Electron Transfer in a Ru(bpy) ₃ ²⁺ –Tyrosine Complex Irebo, Tania; Zhang, Ming-Tian; Markle, Todd F. Journal of the American Chemical Society, Vol. 134, Issue 39 https://doi.org/10.1021/ja3053859	journal	September 2012
Multiple-Site Concerted Proton–Electron Transfer Reactions of Hydrogen-Bonded Phenols Are Nonadiabatic and Well Described by Semiclassical Marcus Theory Schrauben, Joel N.; Cattaneo, Mauricio; Day, Thomas C. Journal of the American Chemical Society, Vol. 134, Issue 40 https://doi.org/10.1021/ja305668h	journal	September 2012
Proton-Coupled Electron Transfers: pH-Dependent Driving Forces? Fundamentals and Artifacts Bonin, Julien; Costentin, Cyrille; Robert, Marc Journal of the American Chemical Society, Vol. 135, Issue 38 https://doi.org/10.1021/ja406712c	journal	September 2013
The Rate Ladder of Proton-Coupled Tyrosine Oxidation in Water: A Systematic Dependence on Hydrogen Bonds and Protonation State Irebo, Tania; Johansson, Olof; Hammarström, Leif Journal of the American Chemical Society, Vol. 130, Issue 29 https://doi.org/10.1021/ja802076v	journal	June 2008
A Bioinspired Construct That Mimics the Proton Coupled Electron Transfer between P680 ^•+ and the Tyr _Z -His190 Pair of Photosystem II Moore, Gary F.; Hambourger, Michael; Gervaldo, Miguel Journal of the American Chemical Society, Vol. 130, Issue 32 https://doi.org/10.1021/ja803015m	journal	August 2008
Proton-Coupled Electron Transfer in Photosystem II: Proton Inventory of a Redox Active Tyrosine Jenson, David L.; Barry, Bridgette A. Journal of the American Chemical Society, Vol. 131, Issue 30 https://doi.org/10.1021/ja902896e	journal	August 2009
Isotope Effects on Hydride Transfer Reactions from Transition Metal Hydrides to Trityl Cation. An Inverse Isotope Effect for a Hydride Transfer Cheng, Tan-Yun; Bullock, R. Morris Journal of the American Chemical Society, Vol. 121, Issue 13 https://doi.org/10.1021/ja983448x	journal	April 1999
EPR Detection of the Transient Tyrosyl Radical in DNA Photolyase from Anacystis nidulans Aubert, Corinne; Brettel, Klaus; Mathis, Paul Journal of the American Chemical Society, Vol. 121, Issue 37 https://doi.org/10.1021/ja991938z	journal	September 1999
Demand-Based Thiolate Anion Generation under Virtually Neutral Conditions: Influence of Steric and Electronic Factors on Chemo- and Regioselective Cleavage of Aryl Alkyl Ethers ^† Chakraborti, Asit K.; Sharma, Lalima; Nayak, Mrinal K. The Journal of Organic Chemistry, Vol. 67, Issue 18 https://doi.org/10.1021/jo0256540	journal	September 2002
Proton-Coupled Electron Transfer Involving Tyrosine Z in Photosystem II ^† Kühne, Henriette; Brudvig, Gary W. The Journal of Physical Chemistry B, Vol. 106, Issue 33 https://doi.org/10.1021/jp0206222	journal	August 2002
Electron Transfer Driven by Proton Fluctuations in a Hydrogen-Bonded Donor−Acceptor Assembly Hodgkiss, Justin M.; Damrauer, Niels H.; Pressé, Steve The Journal of Physical Chemistry B, Vol. 110, Issue 38 https://doi.org/10.1021/jp056703q	journal	June 2006
Proton-Coupled Electron Transfer and Tyrosine D of Photosystem II Jenson, David L.; Evans, Amaris; Barry, Bridgette A. The Journal of Physical Chemistry B, Vol. 111, Issue 43 https://doi.org/10.1021/jp075726x	journal	October 2007
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
Broadband Spectral Probing Revealing Ultrafast Photochemical Branching after Ultraviolet Excitation of the Aqueous Phenolate Anion Chen, Xiyi; Larsen, Delmar S.; Bradforth, Stephen E. The Journal of Physical Chemistry A, Vol. 115, Issue 16 https://doi.org/10.1021/jp107935f	journal	April 2011
Probing Quantum and Dynamic Effects in Concerted Proton–Electron Transfer Reactions of Phenol–Base Compounds Markle, Todd F.; Tenderholt, Adam L.; Mayer, James M. The Journal of Physical Chemistry B, Vol. 116, Issue 1 https://doi.org/10.1021/jp2091736	journal	December 2011
Proton-Coupled Electron Transfer in Tyrosine and a β-Hairpin Maquette: Reaction Dynamics on the Picosecond Time Scale Pagba, Cynthia V.; Chi, San-Hui; Perry, Joseph The Journal of Physical Chemistry B, Vol. 119, Issue 6 https://doi.org/10.1021/jp510171z	journal	August 2014
Analysis of Kinetic Isotope Effects for Proton-Coupled Electron Transfer Reactions ^† Edwards, Sarah J.; Soudackov, Alexander V.; Hammes-Schiffer, Sharon The Journal of Physical Chemistry A, Vol. 113, Issue 10 https://doi.org/10.1021/jp809122y	journal	March 2009
The Kinetic Effect of Internal Hydrogen Bonds on Proton-Coupled Electron Transfer from Phenols: A Theoretical Analysis with Modeling of Experimental Data Johannissen, Linus O.; Irebo, Tania; Sjödin, Martin The Journal of Physical Chemistry B, Vol. 113, Issue 50 https://doi.org/10.1021/jp9048633	journal	December 2009
Contemporary Issues in Electron Transfer Research Barbara, Paul F.; Meyer, Thomas J.; Ratner, Mark A. The Journal of Physical Chemistry, Vol. 100, Issue 31 https://doi.org/10.1021/jp9605663	journal	January 1996
Proton-Coupled Electron Transfer Reactions: Evaluation of Rate Constants Cukier, R. I. The Journal of Physical Chemistry, Vol. 100, Issue 38 https://doi.org/10.1021/jp961025g	journal	January 1996
Evaluation of Solvent Effects in Isotropic and Anisotropic Dielectrics and in Ionic Solutions with a Unified Integral Equation Method: Theoretical Bases, Computational Implementation, and Numerical Applications Mennucci, B.; Cancès, E.; Tomasi, J. The Journal of Physical Chemistry B, Vol. 101, Issue 49 https://doi.org/10.1021/jp971959k	journal	December 1997
New applications of integral equations methods for solvation continuum models: ionic solutions and liquid crystals Cancès, Eric; Mennucci, Benedetta Journal of Mathematical Chemistry, Vol. 23, Issue 3/4, p. 309-326 https://doi.org/10.1023/A:1019133611148	journal	January 1998
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
A phenol–imidazole pro-ligand that can exist as a phenoxyl radical, alone and when complexed to copper( ii ) and zinc( ii ) Benisvy, Laurent; Blake, Alexander J.; Collison, David Dalton Trans., Issue 10 https://doi.org/10.1039/B212209J	journal	January 2003
Steric effect for proton, hydrogen-atom, and hydride transfer reactions with geometric isomers of NADH–model ruthenium complexes Cohen, Brian W.; Polyansky, Dmitry E.; Achord, Patrick Faraday Discuss., Vol. 155 https://doi.org/10.1039/C1FD00094B	journal	January 2012
Proton-coupled electron transfer: classification scheme and guide to theoretical methods Hammes-Schiffer, Sharon Energy & Environmental Science, Vol. 5, Issue 7 https://doi.org/10.1039/c2ee03361e	journal	January 2012
Photochemical tyrosine oxidation with a hydrogen-bonded proton acceptor by bidirectional proton-coupled electron transfer Pizano, Arturo A.; Yang, Jay L.; Nocera, Daniel G. Chemical Science, Vol. 3, Issue 8 https://doi.org/10.1039/c2sc20113e	journal	January 2012
Controlling electron transfer in strong time-dependent fields: Theory beyond the Golden Rule approximation Hartmann, Ludwig; Goychuk, Igor; Hänggi, Peter The Journal of Chemical Physics, Vol. 113, Issue 24 https://doi.org/10.1063/1.1326049	journal	December 2000
Dielectric Relaxation in Alkylcyanides No authors listed The Journal of Chemical Physics, Vol. 41, Issue 3, p. 827-831 https://doi.org/10.1063/1.1725967	journal	August 1964
Multidimensional treatment of stochastic solvent dynamics in photoinduced proton-coupled electron transfer processes: Sequential, concerted, and complex branching mechanisms Soudackov, Alexander V.; Hazra, Anirban; Hammes-Schiffer, Sharon The Journal of Chemical Physics, Vol. 135, Issue 14 https://doi.org/10.1063/1.3651083	journal	October 2011
Ab initio effective core potentials for molecular calculations. Potentials for K to Au including the outermost core orbitals Hay, P. Jeffrey; Wadt, Willard R. The Journal of Chemical Physics, Vol. 82, Issue 1, p. 299-310 https://doi.org/10.1063/1.448975	journal	January 1985
Dynamical effects in electron transfer reactions Sumi, H.; Marcus, R. A. The Journal of Chemical Physics, Vol. 84, Issue 9 https://doi.org/10.1063/1.449978	journal	May 1986
Dynamic solvent effects on outer‐sphere electron transfer Rips, Ilya; Jortner, Joshua The Journal of Chemical Physics, Vol. 87, Issue 4 https://doi.org/10.1063/1.453184	journal	August 1987
Outer sphere electron transfer in polar solvents. Activationless and inverted regimes Rips, Ilya; Jortner, Joshua The Journal of Chemical Physics, Vol. 87, Issue 11 https://doi.org/10.1063/1.453434	journal	December 1987
A new mixing of Hartree–Fock and local density‐functional theories Becke, Axel D. The Journal of Chemical Physics, Vol. 98, Issue 2 https://doi.org/10.1063/1.464304	journal	January 1993
Density‐functional thermochemistry. III. The role of exact exchange Becke, Axel D. The Journal of Chemical Physics, Vol. 98, Issue 7, p. 5648-5652 https://doi.org/10.1063/1.464913	journal	April 1993
A new integral equation formalism for the polarizable continuum model: Theoretical background and applications to isotropic and anisotropic dielectrics Cancès, E.; Mennucci, B.; Tomasi, J. The Journal of Chemical Physics, Vol. 107, Issue 8 https://doi.org/10.1063/1.474659	journal	August 1997
Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor Holzwarth, A. R.; Muller, M. G.; Reus, M. Proceedings of the National Academy of Sciences, Vol. 103, Issue 18 https://doi.org/10.1073/pnas.0505371103	journal	April 2006
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
The electrochemical approach to concerted proton--electron transfers in the oxidation of phenols in water Costentin, C.; Louault, C.; Robert, M. Proceedings of the National Academy of Sciences, Vol. 106, Issue 43 https://doi.org/10.1073/pnas.0910065106	journal	October 2009
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
Picosecond kinetics of fluorescence and absorbance changes in photosystem II particles excited at low photon density Schatz, G. H.; Brock, H.; Holzwarth, A. R. Proceedings of the National Academy of Sciences, Vol. 84, Issue 23 https://doi.org/10.1073/pnas.84.23.8414	journal	December 1987
Chemical complementation identifies a proton acceptor for redox-active tyrosine D in photosystem II Kim, S.; Liang, J.; Barry, B. A. Proceedings of the National Academy of Sciences, Vol. 94, Issue 26 https://doi.org/10.1073/pnas.94.26.14406	journal	December 1997
Intraprotein electron transfer between tyrosine and tryptophan in DNA photolyase from Anacystis nidulans Aubert, C.; Mathis, P.; Eker, A. P. M. Proceedings of the National Academy of Sciences, Vol. 96, Issue 10 https://doi.org/10.1073/pnas.96.10.5423	journal	May 1999
Density-functional exchange-energy approximation with correct asymptotic behavior Becke, A. D. Physical Review A, Vol. 38, Issue 6 https://doi.org/10.1103/PhysRevA.38.3098	journal	September 1988
Development of the Colle-Salvetti correlation-energy formula into a functional of the electron density Lee, Chengteh; Yang, Weitao; Parr, Robert G. Physical Review B, Vol. 37, Issue 2 https://doi.org/10.1103/PhysRevB.37.785	journal	January 1988
COOPERATION OF CHARGES IN PHOTOSYNTHETIC O ₂ EVOLUTION–I. A LINEAR FOUR STEP MECHANISM Kok, Bessel; Forbush, Bliss; McGLOIN, Marion Photochemistry and Photobiology, Vol. 11, Issue 6 https://doi.org/10.1111/j.1751-1097.1970.tb06017.x	journal	June 1970
Photosynthetic O2 Formation Tracked by Time-Resolved X-ray Experiments Haumann, M. Science, Vol. 310, Issue 5750 https://doi.org/10.1126/science.1117551	journal	November 2005
Polar Solvent Dynamics and Electron-Transfer Reactions Maroncelli, M.; Macinnis, J.; Fleming, G. R. Science, Vol. 243, Issue 4899 https://doi.org/10.1126/science.243.4899.1674	journal	March 1989
Photosystem II: The Reaction Center of Oxygenic Photosynthesis Vinyard, David J.; Ananyev, Gennady M.; Charles Dismukes, G. Annual Review of Biochemistry, Vol. 82, Issue 1 https://doi.org/10.1146/annurev-biochem-070511-100425	journal	June 2013
Electron Transfer Reactions in Condensed Phases Newton, M. D.; Sutin, N. Annual Review of Physical Chemistry, Vol. 35, Issue 1 https://doi.org/10.1146/annurev.pc.35.100184.002253	journal	October 1984

Cited By (15)

New Properties of a Bioinspired Pyridine Benzimidazole Compound as a Novel Differential Staining Agent for Endoplasmic Reticulum and Golgi Apparatus in Fluorescence Live Cell Imaging Llancalahuen, Felipe M.; Fuentes, Juan A.; Carreño, Alexander Frontiers in Chemistry, Vol. 6 https://doi.org/10.3389/fchem.2018.00345	journal	August 2018
Metal Organic Framework Derived Materials: Progress and Prospects for the Energy Conversion and Storage Indra, Arindam; Song, Taeseup; Paik, Ungyu Advanced Materials, Vol. 30, Issue 39 https://doi.org/10.1002/adma.201705146	journal	July 2018
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, Vol. 130, Issue 29 https://doi.org/10.1002/ange.201804498	journal	June 2018
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
Highly Polarized Coumarin Derivatives Revisited: Solvent‐Controlled Competition Between Proton‐Coupled Electron Transfer and Twisted Intramolecular Charge Transfer Morawski, Olaf W.; Kielesiński, Łukasz; Gryko, Daniel T. Chemistry – A European Journal, Vol. 26, Issue 32 https://doi.org/10.1002/chem.202001079	journal	May 2020
Excited State Interaction of Ruthenium (II) Imidazole Phenanthroline Complex [Ru(bpy) ₂ ipH] ²⁺ with 1,4‐Benzoquinone: Simple Electron Transfer or Proton‐Coupled Electron Transfer? Khade, Rahul V.; Dutta Choudhury, Sharmistha; Pal, Haridas ChemPhysChem, Vol. 19, Issue 18 https://doi.org/10.1002/cphc.201800313	journal	June 2018
Ruthenium(II)-Pyridylimidazole Complexes as Photoreductants and PCET Reagents: Ruthenium(II)-Pyridylimidazole Complexes as Photoreductants and PCET Reagents Pannwitz, Andrea; Prescimone, Alessandro; Wenger, Oliver S. European Journal of Inorganic Chemistry, Vol. 2017, Issue 3 https://doi.org/10.1002/ejic.201601403	journal	January 2017
Axial Ligand Effects of Ru-BDA Complexes in the O-O Bond Formation via the I2M Bimolecular Mechanism in Water Oxidation Catalysis: Axial Ligand Effects of Ru-BDA Complexes in the O-O Bond Formation via the I2M Bimolecular Mechanism in Water Oxidation Catalysis Richmond, Craig J.; Escayola, Sílvia; Poater, Albert European Journal of Inorganic Chemistry, Vol. 2019, Issue 15 https://doi.org/10.1002/ejic.201801450	journal	February 2019
A ferrocene∩europium assembly showing phototriggered anticancer activity and fluorescent modality imaging Qu, Jian; Xia, Qing; Ji, Wei Dalton Transactions, Vol. 47, Issue 5 https://doi.org/10.1039/c7dt04492e	journal	January 2018
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
Theoretical analysis of the inverted region in photoinduced proton-coupled electron transfer Goldsmith, Zachary K.; Soudackov, Alexander V.; Hammes-Schiffer, Sharon Faraday Discussions, Vol. 216 https://doi.org/10.1039/c8fd00240a	journal	January 2019
Excited state structural dynamics of 4-cyano-4′-hydroxystilbene: deciphering the signatures of proton-coupled electron transfer using ultrafast Raman loss spectroscopy Mathew, Reshma; Kayal, Surajit; Yapamanu, Adithya Lakshmanna Physical Chemistry Chemical Physics, Vol. 21, Issue 40 https://doi.org/10.1039/c9cp02923k	journal	January 2019
A photochemical and theoretical study of the triplet reactivity of furano- and pyrano-1,4-naphthoquionones towards tyrosine and tryptophan derivatives Teixeira, Rodolfo I.; Goulart, Juliana S.; Corrêa, Rodrigo J. RSC Advances, Vol. 9, Issue 24 https://doi.org/10.1039/c9ra01939a	journal	January 2019
Signatures of vibronic coupling in two-dimensional electronic-vibrational and vibrational-electronic spectroscopies Gaynor, James D.; Khalil, Munira The Journal of Chemical Physics, Vol. 147, Issue 9 https://doi.org/10.1063/1.4991745	journal	September 2017
A stable dye-sensitized photoelectrosynthesis cell mediated by a NiO overlayer for water oxidation Wang, Degao; Niu, Fujun; Mortelliti, Michael J. Proceedings of the National Academy of Sciences, Vol. 117, Issue 23 https://doi.org/10.1073/pnas.1821687116	journal	September 2019