Evidence for Asymmetric Electron Transfer in Cyanobacterial Photosystem I: Analysis of a Methionine-to-Leucine Mutation of the Ligand to the Primary Electron Acceptor A0

Rachel O. Cohen, Gaozhong Shen, John H. Golbeck, Wu Xu, Parag R. Chitnis, Alfia I. Valieva, Art Van Der Est, Yulia Pushkar, Dietmar Stehlik

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Abstract

The X-ray crystal structure of photosystem I (PS I) depicts six chlorophyll a molecules (in three pairs), two phylloquinones, and a [4Fe-4S] cluster arranged in two pseudo C2-symmetric branches that diverge at the P700 special pair and reconverge at the interpolypeptide F x cluster. At present, there is agreement that light-induced electron transfer proceeds via the PsaA branch, but there is conflicting evidence whether, and to what extent, the PsaB branch is active. This problem is addressed in cyanobacterial PS I by changing Met688PsaA and Met668PsaB, which provide the axial ligands to the Mg2+ of the eC-A3 and eC-B3-chlorophylls, to Leu. The premise of the experiment is that alteration or removal of the ligand should alter the midpoint potential of the A0-/A0 redox pair and thereby result in a change in the forward electron-transfer kinetics from A0- to A 1. In comparison with the wild type, the PsaA-branch mutant shows: (i) slower growth rates, higher light sensitivity, and reduced amounts of PS I; (ii) a reduced yield of electron transfer from P700 to the F A/FB iron-sulfur clusters at room temperature; (iii) an increased formation of the 3P700 triplet state due to P700+A0- recombination; and (iv) a change in the intensity and shape of the polarization patterns of the consecutive radical pair states P700+A1- and P700+F x-. The latter changes are temperature dependent and most pronounced at 298 K. These results are interpreted as being due to disorder in the A0 binding site, which leads to a distribution of lifetimes for A0- in the PsaA branch of cofactors. This allows a greater degree of singlet-triplet mixing during the lifetime of the radical pair P700+A0-, which changes the polarization patterns of P700+A1- and P700+F x-. The lower quantum yield of electron transfer is also the likely cause of the physiological changes in this mutant. In contrast, the PsaB-branch mutant showed only minor changes in its physiological and spectroscopic properties. Because the environments of eC-A3 and eC-B3 are nearly identical, these results provide evidence for asymmetric electron-transfer activity primarily along the PsaA branch in cyanobacterial PS I.

Original languageEnglish (US)
Pages (from-to)4741-4754
Number of pages14
JournalBiochemistry
Volume43
Issue number16
DOIs
StatePublished - Apr 27 2004

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All Science Journal Classification (ASJC) codes

  • Biochemistry

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