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 Å for [P(700)(+)A(1A)(-)] and 24.25 ± 0.01 Å 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 prokaryotes 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.
Santabarbara
Stefano
S
Department of Biology, University College London, Gower Street, London WC1E 6BT, United Kingdom. stefano.santabarbara@cnr.it
Kuprov
Ilya
I
Poluektov
Oleg
O
Casal
Antonio
A
Russell
Charlotte A
CA
Purton
Saul
S
Evans
Michael C W
MC
D003080:Cold Temperature; D004578:Electron Spin Resonance Spectroscopy; D004579:Electron Transport; D008954:Models, Biological; D008958:Models, Molecular; D009154:Mutation; D010084:Oxidation-Reduction; D045322:Photosynthetic Reaction Center Complex Proteins / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D045331:Photosystem I Protein Complex / Q000737:chemistry* / Q000378:metabolism*; D046939:Synechocystis / Q000737:chemistry / Q000378:metabolism / Q000648:ultrastructure
D045322:Photosynthetic Reaction Center Complex Proteins; D045331:Photosystem I Protein Complex