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Changes in the Electron Transfer Symmetry in the Photosystem I Reaction Centers upon Removal of Iron–Sulfur Clusters

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Abstract

In photosynthetic reaction centers of intact photosystem I (PSI) complexes from cyanobacteria, electron transfer at room temperature occurs along two symmetrical branches of redox cofactors A and B at a ratio of ~3 : 1 in favor of branch A. Previously, this has been indirectly demonstrated using pulsed absorption spectroscopy and more directly by measuring the decay modulation frequencies of electron spin echo signals (electron spin echo envelope modulation, ESEEM), which allows to determine the distance between the separated charges of the primary electron donor P700+ and phylloquinone acceptors A1A– and A1B– in the symmetric redox cofactors branches A and B. In the present work, these distances were determined using ESEEM in PSI complexes lacking three 4Fe–4S clusters, FX, FA, and FB, and the PsaC protein subunit (the so-called P700–A1 core), in which phylloquinone molecules A1A and A1B serve as the terminal electron acceptors. It was shown that in the P700–A1 core preparations, the average distance between the centers of the P700+A1– ion-radical pair at a temperature of 150 K in an aqueous glycerol solution and in a dried trehalose matrix, as well as in a trehalose matrix at 280 K, is ~25.5 Å, which corresponds to the symmetrical electron transfer along the A and B branches of redox cofactors at a ratio of 1 : 1. Possible reasons for the change in the electron transfer symmetry in PSI upon removal of the PsaC subunit and 4Fe–4S clusters FX, FA, and FB are discussed.

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Abbreviations

A1 :

phylloquinone, secondary electron acceptor

Chl:

chlorophyll

Em :

midpoint redox potential

ESEEM:

electron spin echo envelope modulation

P700 :

chlorophyll dimer, primary electron donor

PhQ:

phylloquinone

PSI:

photosystem I

RC:

reaction center

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Acknowledgments

This work is dedicated to the memory of the outstanding scientist in the field of primary photosynthetic reactions – Vladimir Anatolyevich Shuvalov. V. A. Shuvalov made an invaluable contribution to the study of the mechanisms of primary reactions in PSI, including the mechanisms of the phylloquinone acceptor A1 reduction. Three co-authors of this article (M.M., G.M., and A.S.) were co-authors of many works by V. A. Shuvalov over the past 15 years and gratefully recall the period of their collaboration with V. A. Shuvalov as exceptionally interesting and productive.

Funding

The study was supported by the Russian Science Foundation and by the Cabinet of Ministers of the Republic of Tatarstan within the framework of the scientific project no. 22-23-20165 (https://rscf.ru/project/22-23-20165/).

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Authors and Affiliations

  1. Zavoisky Physical-Technical Institute, FRC Kazan Scientific Center, Russian Academy of Sciences, 420029, Kazan, Russia

    Andrey A. Sukhanov & Kev M. Salikhov

  2. Belozersky Institute of Physico-Chemical Biology, Lomonosov Moscow State University, 119234, Moscow, Russia

    Mahir D. Mamedov, Georgy E. Milanovsky & Alexey Yu. Semenov

Authors
  1. Andrey A. Sukhanov
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  2. Mahir D. Mamedov
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  3. Georgy E. Milanovsky
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  4. Kev M. Salikhov
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  5. Alexey Yu. Semenov
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Contributions

M. D. Mamedov and G. E. Milanovsky isolated PSI complexes; A. A. Sukhanov and K. M. Salikhov recorded EPR spectra; A. Yu. Semenov developed the concept, supervised the study, and wrote the article; M. D. Mamedov, G. E. Milanovsky, A. A. Sukhanov, K. M. Salikhov, and A. Yu. Semenov discussed the results and edited the manuscript.

Corresponding author

Correspondence to Alexey Yu. Semenov.

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The authors declare no conflict of interest in financial or any other sphere. This article does not contain description of studies with human participants or animals performed by any of the authors.

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Sukhanov, A.A., Mamedov, M.D., Milanovsky, G.E. et al. Changes in the Electron Transfer Symmetry in the Photosystem I Reaction Centers upon Removal of Iron–Sulfur Clusters. Biochemistry Moscow 87, 1109–1118 (2022). https://doi.org/10.1134/S0006297922100042

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