Directionality of Electron-Transfer Reactions in Photosystem I of Prokaryotes: Universality of the Bidirectional Electron-Transfer Model

The electron-transfer (ET) reactions in photosystem I (PS I) of prokaryotes have been investigated in wild-type cells of the cyanobacterium Synechocystis sp. PCC 6803, and in two site-directed mutants in which the methionine residue of the reaction center subunits PsaA and PsaB, which acts as the axial ligand to the primary electron chlorophyll acceptor A 0 , was substituted with histidine. Analysis by pulsed electron paramagnetic resonance spectroscopy at 100 K indicates the presence of two forms of the secondary spin-correlated radical pairs, which are assigned to [P 700 + A 1A - ] and [P 700 + A 1B - ], where A 1A and A 1B are the phylloquinone molecules bound to the PsaA and the PsaB reaction center subunits, respectively. Each of the secondary radical pair forms is selectively observed in either the PsaA-M688H or the PsaB-M668H mutant, whereas both radical pairs are observed in the wild type following reduction of the iron-sulfur cluster F X , the intermediate electron acceptor between A 1 and the terminal acceptors F A and F B . Analysis of the time and spectral dependence of the light-induced electron spin echo allows the resolution of structural differences between the [P 700 +A 1A - ] and [P 700 + A 1B - ] radical pairs. The interspin distance is 25.43 ± 0.01 A for [P 700 + A 1A - ] and 24.25 ± 0.01 A for [P 700 + A 1B ]. Moreover, the relative orientation of the interspin vector is rotated by ∼60° with respect to the g-tensor of the P 700 + radical. These estimates are in agreement with the crystallographic structural model, indicating that the cofactors bound to both reaction center subunits of prokaryotic PS I are actively involved in electron transport. This work supports the model that bidirectionality is a general property of type I reaction centers from both prokaryoles and eukaryotes, and contrasts with the situation for photosystem II and other type II reaction centers, in which ET is strongly asymmetric. A revised model that explains qualitatively the heterogeneity of ET reactions at cryogenic temperatures is discussed.