Current state of the primary charge separation mechanism in photosystem I of cyanobacteria

Abstract

This review analyzes new data on the mechanism of ultrafast reactions of primary charge separation in photosystem I (PS I) of cyanobacteria obtained in the last decade by methods of femtosecond absorption spectroscopy. Cyanobacterial PS I from many species harbours 96 chlorophyll a (Chl a) molecules, including six specialized Chls denoted Chl_1A/Chl_1B (dimer P₇₀₀, or P_AP_B), Chl_2A/Chl_2B, and Chl_3A/Chl_3B arranged in two branches, which participate in electron transfer reactions. The current data indicate that the primary charge separation occurs in a symmetric exciplex, where the special pair P₇₀₀ is electronically coupled to the symmetrically located monomers Chl_2A and Chl_2B, which can be considered together as a symmetric exciplex Chl_2AP_AP_BChl_2B with the mixed excited (Chl_2AP_AP_BChl_2B)^* and two charge-transfer states P₇₀₀ ⁺Chl_2A ^- and P₇₀₀ ⁺Chl_2B ^-. The redistribution of electrons between the branches in favor of the A-branch occurs after reduction of the Chl_2A and Chl_2B monomers. The formation of charge-transfer states and the symmetry breaking mechanisms were clarified by measuring the electrochromic Stark shift of β-carotene and the absorption dynamics of PS I complexes with the genetically altered Chl _2B or Chl _2A monomers. The review gives a brief description of the main methods for analyzing data obtained using femtosecond absorption spectroscopy. The energy levels of excited and charge-transfer intermediates arising in the cyanobacterial PS I are critically analyzed.

Keywords: Electron transfer; Femtosecond absorption spectroscopy; Photosystem I; Primary charge separation.

Fig. 1

Cofactors of the monomeric PS I complex from the cyanobacterium Thermosynechococcus elongatus (Jordan et al. 2001). Shown are macrocycles of chlorophyll molecules in the antenna (PsaA subunit - magenta, PsaB - violet, peripheral subunits - gray) and the reaction center (P₇₀₀ - yellow, Chl₂ - orange, Chl₃ - mulberry), b-carotene molecules (light blue), and heterocycles of phylloquinone A₁ (green). The cross denotes the C₃-symmetry axis of the trimer supercomplex. The red arrows mark the main pathways for the excitation energy transfer from the antenna to the reaction center (Byrdin et al. ; Kramer et al. 2018)

Fig. 2

Two branches of redox-active cofactors and the bifurcating electronic transitions in the RC of PS I. A. The cofactors include symmetrical pairs of chlorophyll P_A/P_B (yellow), Chl_2A/Chl_2B (orange), Chl_3A/Chl_3B (red), and phylloquinone A_1A/A_1B (green). Water molecules (silver spheres) coordinated by the PsaA-N600 and PsaB-N582 asparagine side chains (cyan) serve as the axial ligands to Chl_2B and Chl_2A. B. The bifurcated kinetic scheme illustrates the key role of the symmetric tetrameric exciplex Chl_2AP_AP_BChl_2B (red box) in which the excited state (Chl_2AP_AP_BChl_2B)* is quantum mechanically mixed with two charge-transfer states P₇₀₀⁺Chl_2A⁻ and P₇₀₀⁺Chl_2B⁻. A redistribution of the unpaired electron between the two branches in favor of the A-branch takes place in the picosecond time scale

Scheme 1

Energy and charge transfer reactions in PS I from Spinacea oleracea, adapted from (White et al., 1996)

Scheme 2

Suggested charge separation mechanisms for a) RC from C. reinhardtii and cyanobacterial PS I (Gibasiewicz et al. ; Melkozernov 2001); b) RC from Synechocystis sp. PCC 6803 (Savikhin et al. 2000) c) revised scheme for RC from Synechocystis sp. PCC 6803 (Savikhin et al. 2001) d) cyanobacterial PS I (Gobets et al. , ; Gobets and Van Grondelle 2001)

Scheme 3

Complementary interpretations of transient spectral intermediates and characteristic times of main electronic transitions in PS I core particles from C. reinhardtii. Adapted from (Müller et al. 2003)

Fig. 3

Transient absorption spectra of PS I from Synechocystis sp. PCC 6803 by application of pump–probe technique with 20-fs low-energy pump pulses centered at 700 nm (A) and at 720 nm (B). Arrows indicate two bleach peaks arising under excitation at 720 nm. These bleach peaks suggest bleaching of P₇₀₀ (~705 nm) and A₀ (~690 nm)

Fig. 4

Decay-associated spectra of the transient absorption dynamics of PS I from Synechocystis sp. PCC 6803 upon excitation at 690 nm (A) and 720 nm (B)

Fig. 5

Effective energy profiles along the reaction coordinate in the adiabatic model of PS I. Diabatic energy terms for ground (black solid), excited (blue dashed) and CT (green and red dashed) states were calculated with parameters ΔG0 = −0.06 eV, λ =0.12 eV, U0 = 1.8 eV; the adiabatic terms with |Vab| =0.1 eV. Bars show the Boltzmann thermal distribution in the ground state. Adapted from (Cherepanov et al. 2017a)

Fig. 6

Free energy levels of various electronic states in the cyanobacterial PS I. Arrows indicate main electronic transitions. Operating redox potentials of the cofactors participating in charge separation are shown on the vertical axis vs SHE