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

Journal name:
Nature Chemistry
Year published:
Published online


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


  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.


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[,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[,6.18,11.113,16]tetracosa-1,3(24),4,6,8,10,12,14,16(22),17,19-undecaen-2-yl}benzoate


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Author information


  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


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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    Crystallographic data for compound dyad-2.

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