A bioinspired redox relay that mimics radical interactions of the Tyr–His pairs of photosystem II

Journal name:
Nature Chemistry
Volume:
6,
Pages:
423–428
Year published:
DOI:
doi:10.1038/nchem.1862
Received
Accepted
Published online

Abstract

In water-oxidizing photosynthetic organisms, light absorption generates a powerfully oxidizing chlorophyll complex (P680•+) in the photosystem II reaction centre. This is reduced via an electron transfer pathway from the manganese-containing water-oxidizing catalyst, which includes an electron transfer relay comprising a tyrosine (Tyr)–histidine (His) pair that features a hydrogen bond between a phenol group and an imidazole group. By rapidly reducing P680•+, the relay is thought to mitigate recombination reactions, thereby ensuring a high quantum yield of water oxidation. Here, we show that an artificial reaction centre that features a benzimidazole–phenol model of the Tyr–His pair mimics both the short-internal hydrogen bond in photosystem II and, using electron paramagnetic resonance spectroscopy, the thermal relaxation that accompanies proton-coupled electron transfer. Although this artificial system is much less complex than the natural one, theory suggests that it captures the essential features that are important in the function of the relay.

At a glance

Figures

  1. Bioinspired triad-1 consisting of three covalently linked redox subunits.
    Figure 1: Bioinspired triad-1 consisting of three covalently linked redox subunits.

    Upon irradiation (1, hν), the system is able to undergo a primary electron transfer reaction (2, ET) and a proton-coupled electron transfer (3, PCET) reaction.

  2. Photoinduced D-band (130 GHz) EPR spectra of an acetonitrile suspension of triad-1 recorded at 13 K.
    Figure 2: Photoinduced D-band (130 GHz) EPR spectra of an acetonitrile suspension of triad-1 recorded at 13 K.

    Purple: immediately after sample illumination in the cavity of the spectrometer. Green: after the illuminated sample has been annealed at 100 K in the dark for 10 min and cooled back to 13 K. Black: theoretical simulation (see Methods).

  3. Crystal structure of dyad-2.
    Figure 3: Crystal structure of dyad-2.

    Carbon is shown in grey, oxygen in red, nitrogen in blue and fluorine in green. On the right, a partial structure of dyad-2 is shown where the t-butyl group ortho to the phenol and part of the porphyrin have been deleted to better visualize the dihedral angle between the phenol and imidazole groups.

  4. Partial 1H NMR spectra of dyad-2.
    Figure 4: Partial 1H NMR spectra of dyad-2.

    The spectra were obtained at 298 K, 500 MHz, in three different deuterated solvents: acetonitrile (top), acetone (middle) and chloroform (bottom).

  5. Calculated structures of the radical cation of the organic component of triad-1.
    Figure 5: Calculated structures of the radical cation of the organic component of triad-1.

    Structure A+ before thermal relaxation and structure B+ after thermal relaxation. Structure A+ includes water molecules hydrogen-bonded to the distal N–H and the phenoxyl oxygen and structure B+ includes water molecules hydrogen-bonded at both distal and proximal N–H sites (see text). Carbon is shown in grey, hydrogen in white, nitrogen in blue, fluorine in cyan and oxygen in red.

Compounds

1 compounds View all compounds
  1. Methyl 4-{12-[3-(1H-1,3-benzodiazol-2-yl)-5-tert-butyl-4-hydroxyphenyl]-7,17-bis(pentafluorophenyl)-21,22,23,24-tetraazapentacyclo[16.2.1.13,6.18,11.113,16]tetracosa-1,3(24),4,6,8,10,12,14,16(22),17,19-undecaen-2-yl}benzoate
    Compound dyad-2 Methyl 4-{12-[3-(1H-1,3-benzodiazol-2-yl)-5-tert-butyl-4-hydroxyphenyl]-7,17-bis(pentafluorophenyl)-21,22,23,24-tetraazapentacyclo[16.2.1.13,6.18,11.113,16]tetracosa-1,3(24),4,6,8,10,12,14,16(22),17,19-undecaen-2-yl}benzoate

References

  1. Babcock, G. T. et al. Water oxidation in photosystem II: from radical chemistry to multielectron chemistry. Biochemistry 28, 95579565 (1989).
  2. Zouni, A. et al. Crystal structure of photosystem II from Synechococcus elongatus at 3.8 Å resolution. Nature 409, 739743 (2000).
  3. Umena, Y., Kawakami, K., Shen, J-R. & Kamiya, N. Crystal structure of oxygen-evolving photosystem II at a resolution of 1.9 Å. Nature 473, 5560 (2011).
  4. Barry, B. A. & Babcock, G. T. Tyrosine radicals are involved in the photosynthetic oxygen-evolving system. Proc. Natl Acad. Sci. USA 84, 70997103 (1987).
  5. Mamedov, F., Sayre, R. T. & Styring, S. Involvement of histidine 190 on the D1 protein in electron/proton transfer reactions on the donor side of photosystem II. Biochemistry 37, 1424514256 (1998).
  6. Hays, A-M. A., Vassiliev, I. R., Golbeck, J. H. & Debus, R. J. Role of D1-His190 in proton-coupled electron transfer reactions in photosystem II: a chemical complementation study. Biochemistry 37, 1135211365 (1998).
  7. Meyer, T. J., Hang, M., Huynh, V. & Thorp, H. H. The role of proton coupled electron transfer (PCET) in water oxidation by photosystem II. Wiring for protons. Angew. Chem. Int. Ed. 46, 52845304 (2007).
  8. Barry, B. A. Proton coupled electron transfer and redox active tyrosines in photosystem II. J. Photochem. Photobiol. B 104, 6071 (2011).
  9. Hammarstöm, L. & Styring, S. Proton-coupled electron transfer of tyrosines in photosystem II and model systems for artificial photosynthesis: the role of a redox-active link between catalyst and photosensitizer. Energy Environ. Sci. 4, 23792388 (2011).
  10. Styring, S., Sjöholm, J. & Mamedov, F. Two tyrosines that changed the world: interfacing the oxidizing power of photochemistry to water splitting in photosystem II. Biochim. Biophys. Acta 1817, 787 (2012).
  11. Faller, P. et al. Rapid formation of the stable tyrosyl radical in photosystem II. Proc. Natl Acad. Sci. USA 98, 1436814373 (2001).
  12. Rappaport, F. et al. Probing the coupling between proton and electron transfer in photosystem II core complexes containing a 3-fluorotyrosine. J. Am. Chem. Soc. 131, 44254433 (2009).
  13. Stubbe, J. A. & van der Donk, W. A. Protein radicals in enzyme catalysis. Chem. Rev. 98, 705762 (1998).
  14. Faller, P., Rutherford, A. W. & Debus, R. J. Tyrosine D oxidation at cryogenic temperature in photosystem II. Biochemistry 41, 1291412920 (2002).
  15. 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. USA 100, 87328735 (2003).
  16. Gust, D., Moore, T. A. & Moore, A. L. Realizing artificial photosynthesis. Faraday Discuss. 155, 926 (2012).
  17. Gust, D., Moore, T. A. & Moore, A. L. Molecular mimicry of photosynthetic energy and electron transfer. Acc. Chem. Res. 26, 198205 (1993).
  18. Megiatto, J. D. Jr <i>et al.</i> Mimicking the electron transfer chain in photosystem II with a molecular triad thermodynamically capable of water oxidation. Proc. Natl Acad. Sci. USA 109, 1557815583 (2012).
  19. Rajh T., Nedeljkovic J. M., Chen L. X., Poluektov O. & Thurnauer M. C. Improving optical and charge separation properties of nanocrystalline TiO2 by surface modification with vitamin C. J. Phys. Chem. B 103, 35153519 (1999).
  20. Moore, G. F. et al. 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, 1046610467 (2008).
  21. Stone, A. J. g factors of aromatic free radicals. Mol. Phys. 6, 509515 (1963).
  22. Smirnova, T. I., Smirnov, A. I., Paschenko, S. V. & Poluektov, O. G. Geometry of hydrogen bonds formed by lipid bilayer nitroxide probes: a high-frequency pulsed ENDOR/EPR study. J. Am. Chem. Soc. 129, 34763477 (2007).
  23. Orio, M. et al. Geometric and electronic structures of phenoxyl radicals hydrogen bonded to neutral and cationic partners. Chem. Eur. J. 18, 54165429 (2012).
  24. Thomas, F. et al. How single and bifurcated hydrogen bonds influence proton-migration rate constants, redox, and electronic properties of phenoxyl radicals. Angew. Chem. Int. Ed. 43, 594597 (2004).
  25. Benisvy, L. et al. Phenoxyl radicals hydrogen-bonded to imidazolium: analogues of Tyrosyl D of photosystem II: high-field EPR and DFT studies. Angew. Chem. Int. Ed. 44, 53145317 (2005).
  26. Un, S., Atta, M., Fontecave, M. & Rutherford, A. W. g-Values as a probe of the local protein environment: high-field EPR of tyrosyl radicals in ribonucleotide reductase and photosystem II. J. Am. Chem. Soc. 117, 1071310719 (1995).
  27. Un, S., Gerez, C., Elleingand, E. & Fontecave, M. Sensitivity of tyrosyl radical g-values to changes in protein structure: a high-field EPR study of mutants of ribonucleotide reductase. J. Am. Chem. Soc. 123, 30483054 (2001).
  28. Saito, K., Shen, J-R., Ishida, T. & Ishikita, H. Short hydrogen bond between redox-active tyrosine YZ and D1-His190 in the photosystem II crystal structure. Biochemistry 50, 98369844 (2011).
  29. Sibert, R. et al. Proton-coupled electron transfer in a biomimetic peptide as a model of enzyme regulatory mechanisms. J. Am. Chem. Soc. 129, 43934400 (2007).
  30. Markle, T. F., Rhile, I. J., Dipasquale, A. G. & Mayer, J. M. Probing concerted proton–electron transfer in phenol–imidazoles. Proc. Natl Acad. Sci. USA 105, 81858190 (2008).
  31. Costentin, C., Robert, M. & Saveant, J-M. Electrochemical and homogeneous proton-coupled electron transfers: concerted pathways in the one-electron oxidation of a phenol coupled with an intramolecular amine-driven proton transfer. J. Am. Chem. Soc. 128, 45524553 (2006).
  32. Fecenko, C. J., Thorp, H. H. & Meyer, T. J. The role of free energy change in coupled electron–proton transfer J. Am. Chem. Soc. 129, 1509815099 (2007).
  33. Hammes-Schiffer, S. Theory of proton-coupled electron transfer in energy conversion processes. Acc. Chem. Res. 42, 18811889 (2009).
  34. Perrin, C. L. & Nielson, J. B. ‘Strong’ hydrogen bonds in chemistry and biology. Annu. Rev. Phys. Chem. 48, 511544 (1997).
  35. Megiatto, J. D. Jr et al. Intramolecular hydrogen bonding as a synthetic tool to induce chemical selectivity in acid catalyzed porphyrin synthesis. Chem. Commun. 48, 45584560 (2012).
  36. Nurminen, E. J., Mattinen, J. K. & Lönnberg, H. Nucleophilic and acid catalysis in phosphoramidite alcoholysis. J. Chem. Soc. Perkin Trans. 2, 21592165 (2001).
  37. Moore, G. F. et al. Effects of protonation state on a tyrosine–histidine bioinspired redox mediator. J. Phys. Chem. B 114, 1445014457 (2010).
  38. Edwards, J. S., Soudackov, A. V. & Hammes-Schiffer, S. Analysis of kinetic isotope effects for proton-coupled electron transfer reactions. J. Phys. Chem. A 113, 21172126 (2009).
  39. Witwicki, M. & Jezierska, J. Protic and aprotic solvent effect on molecular properties and g-tensors of o-semiquinones with various aromacity and heteroatoms: a DFT study. Chem. Phys. Lett. 493, 364370 (2010).
  40. Witwicki, M., Jezierska, J. & Ozarowski, A. Solvent effect on EPR, molecular and electronic properties of semiquinone radical derived from 3,4-dihydroxybenzoic acid as model for humic acid transient radicals: high-field EPR and DFT studies. Chem. Phys. Lett. 473, 160166 (2009).
  41. Barry, B. A. et al. Proton-coupled electron transfer and redox active tyrosines: structure and function of tyrosyl radicals in ribonucleotide reductase and photosystem II. J. Phys. Chem. Lett. 3, 534554 (2012).
  42. Jenson D. L. & Barry, B. A. Proton-coupled electron transfer in photosystem II: proton inventory of a redox active tyrosine. J. Am. Chem. Soc. 131, 1056710573 (2009).
  43. Chatterjee, R. et al. High-frequency electron nuclear double-resonance spectroscopy studies of the mechanism of proton-coupled electron transfer at the tyrosine-D residue of photosystem II. Biochemistry 52, 47814790 (2013).
  44. Zhao, Y. et al. Improving the efficiency of water splitting in dye-sensitized solar cells by using a biomimetic electron transfer mediator. Proc. Natl Acad. Sci. USA 109, 1561215616 (2012).
  45. Rajh, T., Ostafin, A. E., Micic, O. I., Tiede, D. M. & Thurnauer, M. C. Surface modification of small particle TiO2 colloids with cysteine for enhanced photochemical reduction:  an EPR study J. Phys. Chem. 100, 45384545 (1996).
  46. Lakshmi, K. V. et al. High-field EPR study of carotenoid and chlorophyll cation radicals in photosystem II. J. Phys. Chem. B 104, 1044510448 (2000).

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Author information

Affiliations

  1. Department of Chemistry and Biochemistry, Arizona State University, Tempe, Arizona 85287-1604, USA

    • Jackson D. Megiatto Jr,
    • Dalvin D. Méndez-Hernández,
    • Marely E. Tejeda-Ferrari,
    • Anne-Lucie Teillout,
    • Manuel J. Llansola-Portolés,
    • Gerdenis Kodis,
    • Vladimiro Mujica,
    • Thomas L. Groy,
    • Devens Gust,
    • Thomas A. Moore &
    • Ana L. Moore
  2. NanoBio Interface Group, Center for Nanoscale Materials and Chemical Sciences and Engineering Division, Argonne National Laboratory Argonne, Illinois 60439, USA

    • Oleg G. Poluektov &
    • Tijana Rajh
  3. Laboratoire de Chimie Physique, Groupe d'Electrochimie et de Photoélectrochimie, UMR 8000, CNRS, Université Paris-Sud, Batiment 350, 91405 Orsay Cedex, France

    • Anne-Lucie Teillout
  4. Present address: Institute of Chemistry, Campinas State University (UNICAMP), PO Box 6154, Campinas, SP, 13084-861, Brazil

    • Jackson D. Megiatto Jr

Contributions

J.D.M.J., D.G., T.A.M. and A.L.M. designed the research and experiments. J.D.M.J. and M.E.T.J. synthesized and characterized all chemical compounds. J.D.M.J and T.L.G. are responsible for the crystal structure. D.D.M.H. and V.M. conducted theoretical calculations. O.G.P. and T.R. performed EPR experiments. A.L.T. carried out electrochemical measurements. M.J.L.P. and G.K. performed photophysical characterizations. J.D.M.J., D.D.M.H., M.J.L.P., G.K., O.G.P., T.R., V.M., D.G., T.A.M. and A.L.M. analysed and interpreted the data. J.D.M.J., D.D.M.H., D.G., T.A.M. and A.L.M. wrote the manuscript.

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The authors declare no competing financial interests.

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    Crystallographic data for compound dyad-2.

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