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Symmetry breaking in photosystem I: ultrafast optical studies of variants near the accessory chlorophylls in the A- and B-branches of electron transfer cofactors

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Abstract

Femtosecond absorption spectroscopy of Photosystem I (PS I) complexes from the cyanobacterium Synechocystis sp. PCC 6803 was carried out on three pairs of complementary amino acid substitutions located near the second pair of chlorophyll molecules Chl2A and Chl2B (also termed A-1A and A-1B). The absorption dynamics at delays of 0.1–500 ps were analyzed by decomposition into discrete decay-associated spectra and continuously distributed exponential components. The multi-exponential deconvolution of the absorption changes revealed that the electron transfer reactions in the PsaA-N600M, PsaA-N600H, and PsaA-N600L variants near the B-branch of cofactors are similar to those of the wild type, while the PsaB-N582M, PsaB-N582H, and PsaB-N582L variants near the A-branch of cofactors cause significant alterations of the photochemical processes, making them heterogeneous and poorly described by a discrete exponential kinetic model. A redistribution of the unpaired electron between the second and the third monomers Chl2A/Chl2B and Chl3A/Chl3B was identified in the time range of 9–20 ps, and the subsequent reduction of A1 was identified in the time range of 24–70 ps. In the PsaA-N600L and PsaB-N582H/L variants, the reduction of A1 occurred with a decreased quantum yield of charge separation. The decreased quantum yield correlates with a slowing of the phylloquinone A0 → A1 reduction, but not with the initial transient spectra measured at the shortest time delay. The results support a branch competition model, where the electron is sheared between Chl2A–Chl3A and Chl2B–Chl3B cofactors before its transfer to phylloquinone in either A1A or A1B sites.

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Acknowledgements

This work was supported by the Russian Science Foundation Grant RSF 19-14-00366 to DAC and AYS and by the US National Science Foundation under grant MCB-1613022 to JHG. Cell growth and isolation of the PS I complexes was funded by NSF EPSCoR (NSF(2010)-PFUND-217) and the Louisiana RCS Program (LEQSF(2013-16)-RD-A-15) to WX. AYS acknowledges partial support from Lomonosov Moscow State University Program of Development. We thank Dr. Vasily Kurashov and Dr. Michael Gorka for valuable discussions.

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Authors and Affiliations

  1. N.N. Semenov Federal Research Center for Chemical Physics, Russian Academy of Sciences, Kosygina St. 4, Moscow, 117977, Russian Federation

    Dmitry A. Cherepanov, Ivan V. Shelaev, Fedor E. Gostev, Victor A. Nadtochenko & Alexey Yu. Semenov

  2. Department of Chemistry, Lomonosov Moscow State University, Leninskiye Gory 1-3, Moscow, 119991, Russian Federation

    Victor A. Nadtochenko

  3. Department of Chemistry, University of Louisiana at Lafayette, Lafayette, LA, 70504, USA

    Wu Xu

  4. Department of Biochemistry and Molecular Biology, The Pennsylvania State University, University Park, PA, 16801, USA

    John H. Golbeck

  5. Department of Chemistry, The Pennsylvania State University, University Park, PA, 16801, USA

    John H. Golbeck

  6. A.N. Belozersky Institute of Physical-Chemical Biology, Lomonosov Moscow State University, Leninskie Gory, 1, Moscow, 119992, Russian Federation

    Alexey Yu. Semenov

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  1. Dmitry A. Cherepanov
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  2. Ivan V. Shelaev
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  5. Wu Xu
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Correspondence to Dmitry A. Cherepanov.

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Pushing the limits of flash photolysis to unravel the secrets of biological electron and proton transfer- a topical issue in honour of Klaus Brettel.

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Cherepanov, D.A., Shelaev, I.V., Gostev, F.E. et al. Symmetry breaking in photosystem I: ultrafast optical studies of variants near the accessory chlorophylls in the A- and B-branches of electron transfer cofactors. Photochem Photobiol Sci 20, 1209–1227 (2021). https://doi.org/10.1007/s43630-021-00094-y

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