Abstract
Photosynthesis powers our planet and is a source of inspiration for developing artificial constructs mimicking many aspects of the natural energy transducing process. In the complex machinery of photosystem II (PSII), the redox activity of the tyrosine Z (Tyrz) hydrogen-bonded to histidine 190 (His190) is essential for its functions. For example, the Tyrz–His190 pair provides a proton-coupled electron transfer (PCET) pathway that effectively competes against the back-electron transfer reaction and tunes the redox potential of the phenoxyl radical/phenol redox couple ensuring a high net quantum yield of photoinduced charge separation in PSII. Herein, artificial assemblies mimicking both the structural and redox properties of the Tyrz–His190 pair are described. The bioinspired constructs contain a phenol (Tyrz model) covalently linked to a benzimidazole (His190 model) featuring an intramolecular hydrogen bond which closely emulates the one observed in the natural counterpart. Incorporation of electron-withdrawing groups in the benzimidazole moiety systematically changes the intramolecular hydrogen bond strength and modifies the potential of the phenoxyl radical/phenol redox couple over a range of ~ 250 mV. Infrared spectroelectrochemistry (IRSEC) demonstrates the associated one-electron, one-proton transfer (E1PT) process upon electrochemical oxidation of the phenol. The present contribution provides insight regarding the factors controlling the redox potential of the phenol and highlights strategies for the design of futures constructs capable of transporting protons across longer distances while maintaining a high potential of the phenoxyl radical/phenol redox couple.
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References
Benisvy L, Bill E, Blake AJ et al (2004) Phenolate and phenoxyl radical complexes of Co(ii) and Co(iii). Dalton Trans 123:3647. https://doi.org/10.1039/b410934a
Benisvy L, Bittl R, Bothe E et al (2005) Phenoxyl radicals hydrogen-bonded to imidazolium: analogues of tyrosyl D· of photosystem II: high-field EPR and DFT studies. Angew Chem Int Ed 44:5314–5317. https://doi.org/10.1002/anie.200501132
Benisvy L, Bill E, Blake AJ et al (2006) Phenoxyl radicals: H-bonded and coordinated to Cu(ii) and Zn(ii). Dalton Trans. https://doi.org/10.1039/B513221P
Connelly NG, Geiger WE (1996) Chemical redox agents for organometallic chemistry. Chem Rev 96:877–910. https://doi.org/10.1021/cr940053x
Das K, Sarkar N, Majumdar D, Bhattacharyya K (1992) Excited-state intramolecular proton transfer and rotamerism of 2-(2′-hydroxyphenyl) benzimidazole. Chem Phys Lett 198:443–448. https://doi.org/10.1016/0009-2614(92)80025-7
Das K, Sarkar N, Ghosh AK et al (1994) Excited-state intramolecular proton transfer in 2-(2-hydroxyphenyl)benzimidazole and -benzoxazole: effect of rotamerism and hydrogen bonding. J Phys Chem 98:9126–9132. https://doi.org/10.1021/j100088a006
Dempsey JL, Winkler JR, Gray HB (2010) Proton-coupled electron flow in protein redox machines. Chem Rev 110:7024–7039. https://doi.org/10.1021/cr100182b
Eckert H-J, Renger G (1988) Temperature dependence of P680 + reduction in O 2 -evolving PS II membrane fragments at different redox states S i of the water oxidizing system. FEBS Lett 236:425–431. https://doi.org/10.1016/0014-5793(88)80070-X
Guerra WD, Odella E, Secor M et al (2020) Role of intact hydrogen-bond networks in multiproton-coupled electron transfer. J Am Chem Soc 142:21842–21851. https://doi.org/10.1021/jacs.0c10474
Guo Z, He J, Barry BA (2018) Calcium, conformational selection, and redox-active tyrosine YZ in the photosynthetic oxygen-evolving cluster. Proc Natl Acad Sci USA 115:5658–5663. https://doi.org/10.1073/pnas.1800758115
Huynh MHV, Meyer TJ (2007) Proton-coupled electron transfer. Chem Rev 107:5004–5064. https://doi.org/10.1021/cr0500030
Huynh MT, Mora SJ, Villalba M et al (2017) Concerted one-electron two-proton transfer processes in models inspired by the Tyr-His couple of photosystem II. ACS Cent Sci 3:372–380. https://doi.org/10.1021/acscentsci.7b00125
Maki T, Araki Y, Ishida Y et al (2001) Construction of persistent phenoxyl radical with intramolecular hydrogen bonding. J Am Chem Soc 123:3371–3372. https://doi.org/10.1021/ja002453+
Mardis KL, Niklas J, Omodayo H et al (2020) One electron multiple proton transfer in model organic donor-acceptor systems: implications for high-frequency EPR. Appl Magn Reson 51:977–991. https://doi.org/10.1007/s00723-020-01252-8
Markle TF, Mayer JM (2008) Concerted proton-electron transfer in pyridylphenols: the importance of the hydrogen bond. Angew Chem Int Ed 47:738–740. https://doi.org/10.1002/anie.200702486
Markle TF, Rhile IJ, DiPasquale AG, Mayer JM (2008) Probing concerted proton-electron transfer in phenol-imidazoles. Proc Natl Acad Sci USA 105:8185–8190. https://doi.org/10.1073/pnas.0708967105
Mathes T, van Stokkum IHM, Stierl M, Kennis JTM (2012) Redox modulation of flavin and tyrosine determines photoinduced proton-coupled electron transfer and photoactivation of BLUF photoreceptors. J Biol Chem 287:31725–31738. https://doi.org/10.1074/jbc.M112.391896
Migliore A, Polizzi NF, Therien MJ, Beratan DN (2014) Biochemistry and theory of proton-coupled electron transfer. Chem Rev 114:3381–3465. https://doi.org/10.1021/cr4006654
Moore GF, Hambourger M, Gervaldo M et al (2008) A bioinspired construct that mimics the proton coupled electron transfer between P680·+ and the TyrZ-His190 pair of photosystem II. J Am Chem Soc 130:10466–10467. https://doi.org/10.1021/ja803015m
Moore GF, Hambourger M, Kodis G et al (2010) Effects of protonation state on a tyrosine-histidine bioinspired redox mediator. J Phys Chem B 114:14450–14457. https://doi.org/10.1021/jp101592m
Mora SJ, Odella E, Moore GF et al (2018) Proton-coupled electron transfer in artificial photosynthetic systems. Acc Chem Res 51:445–453. https://doi.org/10.1021/acs.accounts.7b00491
Mora SJ, Heredia DA, Odella E et al (2019) Design and synthesis of benzimidazole phenol-porphyrin dyads for the study of bioinspired photoinduced proton-coupled electron transfer. J Porphyr Phthalocyanines 23:1336–1345. https://doi.org/10.1142/S1088424619501189
Morgan KJ (1961) The infrared spectra of some simple benzimidazoles. J Chem Soc. https://doi.org/10.1039/JR9610002343
Odella E, Mora SJ, Wadsworth BL et al (2018) Controlling proton-coupled electron transfer in bioinspired artificial photosynthetic relays. J Am Chem Soc 140:15450–15460. https://doi.org/10.1021/jacs.8b09724
Odella E, Wadsworth BL, Mora SJ et al (2019) Proton-coupled electron transfer drives long-range proton translocation in bioinspired systems. J Am Chem Soc 141:14057–14061. https://doi.org/10.1021/jacs.9b06978
Odella E, Mora SJ, Wadsworth BL et al (2020) Proton-coupled electron transfer across benzimidazole bridges in bioinspired proton wires. Chem Sci 11:3820–3828. https://doi.org/10.1039/C9SC06010C
Orio M, Jarjayes O, Baptiste B et al (2012) Geometric and electronic structures of phenoxyl radicals hydrogen bonded to neutral and cationic partners. Chem A 18:5416–5429. https://doi.org/10.1002/chem.201102854
Pannwitz A, Wenger OS (2019) Recent advances in bioinspired proton-coupled electron transfer. Dalton Trans 48:5861–5868. https://doi.org/10.1039/c8dt04373f
Reece SY, Nocera DG (2009) Proton-coupled electron transfer in biology: results from synergistic studies in natural and model systems. Annu Rev Biochem 78:673–699. https://doi.org/10.1146/annurev.biochem.78.080207.092132
Rhile IJ, Mayer JM (2004) One-electron oxidation of a hydrogen-bonded phenol occurs by concerted proton-coupled electron transfer. J Am Chem Soc 126:12718–12719. https://doi.org/10.1021/ja031583q
Rhile IJ, Markle TF, Nagao H et al (2006) Concerted proton−electron transfer in the oxidation of hydrogen-bonded phenols. J Am Chem Soc 128:6075–6088. https://doi.org/10.1021/ja054167+
Richards JA, Whitson PE, Evans DH (1975) Electrochemical oxidation of 2,4,6-tri-tert-butylphenol. J Electroanal Chem Interfacial Electrochem 63:311–327. https://doi.org/10.1016/S0022-0728(75)80303-2
Stubbe J, Nocera DG, Yee CS, Chang MCY (2003) Radical initiation in the class I ribonucleotide reductase: long-range proton-coupled electron transfer? Chem Rev 103:2167–2202. https://doi.org/10.1021/cr020421u
Thomas F, Jarjayes O, Jamet H et al (2004) How single and bifurcated hydrogen bonds influence proton-migration rate constants, redox, and electronic properties of phenoxyl radicals. Angew Chem Int Ed 43:594–597. https://doi.org/10.1002/anie.200352368
Tommos C, Babcock GT (2000) Proton and hydrogen currents in photosynthetic water oxidation. Biochim Biophys Acta 1458:199–219. https://doi.org/10.1016/S0005-2728(00)00069-4
Umena Y, Kawakami K, Shen J-R, Kamiya N (2011) Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473:55–60. https://doi.org/10.1038/nature09913
Webster RD (2003) In situ electrochemical-ATR-FTIR spectroscopic studies on solution phase 2,4,6-tri-substituted phenoxyl radicals. Electrochem Commun 5:6–11. https://doi.org/10.1016/S1388-2481(02)00517-9
Weinberg DR, Gagliardi CJ, Hull JF et al (2012) Proton-coupled electron transfer. Chem Rev 112:4016–4093. https://doi.org/10.1021/cr200177j
Zhang M-T, Irebo T, Johansson O, Hammarström L (2011) Proton-coupled electron transfer from tyrosine: a strong rate dependence on intramolecular proton transfer distance. J Am Chem Soc 133:13224–13227. https://doi.org/10.1021/ja203483j
Zhao Y, Swierk JR, Megiatto JD et al (2012) Improving the efficiency of water splitting in dye-sensitized solar cells by using a biomimetic electron transfer mediator. Proc Natl Acad Sci USA 109:15612–15616. https://doi.org/10.1073/pnas.1118339109
Zhong D (2015) Electron transfer mechanisms of DNA repair by photolyase. Annu Rev Phys Chem 66:691–715. https://doi.org/10.1146/annurev-physchem-040513-103631
Acknowledgements
The research leading to these results received funding from the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Grant DE-FG02-03ER15393.
Funding
The research leading to these results received funding from the U.S. Department of Energy, Office of Science, Office of Basic Energy Sciences, under Grant DE-FG02-03ER15393.
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All authors contributed to the conception and design of the systems. Preparation of the compounds and data collection were performed by EO. Analysis of the data was performed by EO, TAM, and ALM. The first draft of the manuscript was written by EO. All authors contributed to writing the final manuscript.
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Odella, E., Moore, T.A. & Moore, A.L. Tuning the redox potential of tyrosine-histidine bioinspired assemblies. Photosynth Res 151, 185–193 (2022). https://doi.org/10.1007/s11120-020-00815-x
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DOI: https://doi.org/10.1007/s11120-020-00815-x