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The plastoquinol–plastoquinone exchange mechanism in photosystem II: insight from molecular dynamics simulations

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Abstract

In the photosystem II (PSII) of oxygenic photosynthetic organisms, the reaction center (RC) core mediates the light-induced electron transfer leading to water splitting and production of reduced plastoquinone molecules. The reduction of plastoquinone to plastoquinol lowers PSII affinity for the latter and leads to its release. However, little is known about the role of protein dynamics in this process. Here, molecular dynamics simulations of the complete PSII complex embedded in a lipid bilayer have been used to investigate the plastoquinol release mechanism. A distinct dynamic behavior of PSII in the presence of plastoquinol is observed which, coupled to changes in charge distribution and electrostatic interactions, causes disruption of the interactions seen in the PSII–plastoquinone complex and leads to the “squeezing out” of plastoquinol from the binding pocket. Displacement of plastoquinol closes the second water channel, recently described in a 2.9 Å resolution PSII structure (Guskov et al. in Nat Struct Mol Biol 16:334–342, 2009), allowing to rule out the proposed “alternating” mechanism of plastoquinol–plastoquinone exchange, while giving support to the “single-channel” one. The performed simulations indicated a pivotal role of D1-Ser264 in modulating the dynamics of the plastoquinone binding pocket and plastoquinol–plastoquinone exchange via its interaction with D1-His252 residue. The effects of the disruption of this hydrogen bond network on the PSII redox reactions were experimentally assessed in the D1 site-directed mutant Ser264Lys.

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Acknowledgments

This work was supported by the COST Action TD1102 “PHOTOTECH. Photosynthetic proteins for technological applications: biosensors and biochips” and by the grant ASI Photosynchlamy n 2013-068-R0 to M.T.G.. MD simulations were supported by standard high-performance computing grants from CASPUR. C. reinhardtii PSII D1 S264 K mutant was kindly provided by Prof. Udo Johanningmeier and Dr. Ivo Bertalan from the Institute of Plant Physiology, Martin Luther University, Halle-Wittenberg (Germany).

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    Authors and Affiliations

    1. Theoretical Biology and Bioinformatics Laboratory, Department of Sciences, Roma Tre University, Viale G. Marconi 446, 00146, Rome, Italy

      Veranika Zobnina & Fabio Polticelli

    2. Institute of Crystallography CNR, 00015, Monterotondo Scalo, Rome, Italy

      Maya D. Lambreva, Giuseppina Rea, Gaetano Campi, Amina Antonacci, Viviana Scognamiglio & Maria Teresa Giardi

    3. National Institute of Nuclear Physics, Roma Tre Section, 00146, Rome, Italy

      Fabio Polticelli

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    1. Veranika Zobnina
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    Correspondence to Fabio Polticelli.

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    Veranika Zobnina and Maya D. Lambreva contributed equally to this work.

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    Zobnina, V., Lambreva, M.D., Rea, G. et al. The plastoquinol–plastoquinone exchange mechanism in photosystem II: insight from molecular dynamics simulations. Photosynth Res 131, 15–30 (2017). https://doi.org/10.1007/s11120-016-0292-4

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