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

Nature Chemistry volume 6, pages 423–428 (2014)Cite this article

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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.

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Figure 1: Bioinspired triad-1 consisting of three covalently linked redox subunits.
Figure 4: Partial 1H NMR spectra of dyad-2.
Figure 2: Photoinduced D-band (130 GHz) EPR spectra of an acetonitrile suspension of triad-1 recorded at 13 K.
Figure 3: Crystal structure of dyad-2.
Figure 5: Calculated structures of the radical cation of the organic component of triad-1.

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Acknowledgements

This work was supported as part of the Center for Bio-Inspired Solar Fuel Production, an Energy Frontier Research Center funded by the US Department of Energy, Office of Science, Office of Basic Energy Sciences (award DE-SC0001016). D.D.M.H. was supported by the National Science Foundation Graduate Research Fellowship Program (NSF-GRFP; grant no. DGE-0802261), by the More Graduate Education at Mountain States Alliance (MGE@MSA) and by the Alliance for Graduate Education and the Professoriate (AGEP), National Science Foundation Cooperative agreement no. HRD-0450137. The high-frequency EPR work was supported by the US Department of Energy, Office of Basic Energy Sciences, Division of Chemical Sciences, Geosciences, and Biosciences (contract no. DE-AC02-06CH11357, O.G.P.). The work performed at the Center for Nanoscale Materials was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences (contract no. DE-AC02-06CH11357).

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  1. Jackson D. Megiatto Jr

    Present address: Present address: Institute of Chemistry, Campinas State University (UNICAMP), PO Box 6154, Campinas, SP, 13084-861, Brazil,

Authors and Affiliations

  1. Department of Chemistry and Biochemistry, Arizona State University, Tempe, 85287-1604, Arizona, 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. Center for Nanoscale Materials and Chemical Sciences and Engineering Division, NanoBio Interface Group, Argonne National Laboratory Argonne, 60439, Illinois, 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

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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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Correspondence to Ana L. Moore.

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Crystallographic data for compound dyad-2. (CIF 47 kb)

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Megiatto Jr, J., Méndez-Hernández, D., Tejeda-Ferrari, M. et al. A bioinspired redox relay that mimics radical interactions of the Tyr–His pairs of photosystem II. Nature Chem 6, 423–428 (2014). https://doi.org/10.1038/nchem.1862

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