Bidirectional Electron Transfer in Photosystem I:  Determination of Two Distances between P700+ and A1- in Spin-Correlated Radical Pairs

Santabarbara, Stefano; Kuprov, Ilya; Fairclough, Wendy V.; Purton, Saul; Hore, P. J.; Heathcote, Peter; Evans, Mike C.W.

doi:10.1021/bi048445d

Cited by 89 publications

(159 citation statements)

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“…A 1A Á -pair to the distance typical for the P 700 Á ? A 1B Á -pair, as observed by Poluektov and coworkers [21] and by Santabarbara and coworkers [26,27], may be explained by a block in electron transfer through the A-branch. This is probably a result of reduction of A 1A with dithionite and illumination (note that the more reducing A 1B cofactor remains oxidized).…”

Section: Discussionmentioning

confidence: 70%

“…The difference in the two distances is in agreement with the difference in the P 700 -to-A 1A and P 700 -to-A 1B distances according to the X-ray diffraction data. An intermediate value of 25.0 Å was obtained in the WT membranes, which was offered as evidence for bidirectional electron transfer [26]. Ultrafast transient absorbance measurements showed that the A 0 -minus A 0 difference signal accumulates in both the M688H PsaA and M668H PsaB mutants, indicating that electron transfer from A 0 Á -to A 1 is blocked or slowed on the appropriate branch [30].…”

Section: Discussionmentioning

confidence: 88%

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Alteration of the Axial Met Ligand to Electron Acceptor A0 in Photosystem I: Effect on the Generation of P 700 ·+ A 1 ·− Radical Pairs as Studied by W-band Transient EPR

et al. 2009

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Photosystem I (PS I) mutants from the cyanobacterium Synechocystis sp. PCC 6803 bearing point mutations to the axial ligands of A 0A (M688N PsaA ) and A 0B (M668N PsaB ) were studied by high-field W-band electron paramagnetic resonance (EPR) spectroscopy. It was found that the EPR observables of PS I from the M668N PsaB mutant were virtual identical to that of the wild type (WT), and are clearly distinct from the M688N PsaA mutant. In particular, the P 700 Á ? decay kinetics in the M688N PsaA mutant is significantly slower than in the WT or the M668N PsaB mutant. The analysis of the out-of-phase electron-electron dipolar electron spin echo envelope modulation shows that in the M668N PsaB mutant, the estimated distance of 26.0 ± 0.3 Å agrees well with the 25.8 Å distance for the P 700 Á ? A 1A Á -radical pair measured in the X-ray crystal structure. In the M688N PsaA mutant, two populations are found with estimated distances of 26.0 ± 0.3 and 25.0 ± 0.3 Å in a ratio of 0.7-0.3, which agree well with the 25.8 Å distance for the P 700 Á ? A 1A Á -radical

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Section: Discussionmentioning

confidence: 70%

Section: Discussionmentioning

confidence: 88%

Alteration of the Axial Met Ligand to Electron Acceptor A0 in Photosystem I: Effect on the Generation of P 700 ·+ A 1 ·− Radical Pairs as Studied by W-band Transient EPR

et al. 2009

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“…However, the fact that the spin density of P 700 þ• is localized on the ec1 B Chl (16) opens the door for distinguishing the P 700 þ PhQ A − and P 700 þ PhQ B − radical pairs (RP) by transient (laser flash-induced) EPR, due to the different relative orientations of the P 700 þ and PhQ − radicals in the two radical pairs. This, indeed, has been observed in PSI prereduced with dithionite (to reduce the FeS clusters), using PSI RCs purified from perdeuterated Synechococcus lividus (17), mutants of C. reinhardtii that affect the axial ligands of the ec3 Chls (18), or in a mutant of Synechocystis sp. PCC6803 targeting the PhQ A site (19).…”

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confidence: 54%

Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center

Müller

Slavov

Luthra

et al. 2010

Proc. Natl. Acad. Sci. U.S.A.

138

218

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Photosystem I (PSI) is a large pigment-protein complex that unites a reaction center (RC) at the core with ∼100 core antenna chlorophylls surrounding it. The RC is composed of two cofactor branches related by a pseudo-C2 symmetry axis. The ultimate electron donor, P 700 (a pair of chlorophylls), and the tertiary acceptor, F X (a Fe 4 S 4 cluster), are both located on this axis, while each of the two branches is made up of a pair of chlorophylls (ec2 and ec3) and a phylloquinone (PhQ). Based on the observed biphasic reduction of F X , it has been suggested that both branches in PSI are competent for electron transfer (ET), but the nature and rate of the initial electron transfer steps have not been established. We report an ultrafast transient absorption study of Chlamydomonas reinhardtii mutants in which specific amino acids donating H-bonds to the 13 1 -keto oxygen of either ec3 A (PsaA-Tyr696) or ec3 B (PsaBTyr676) are converted to Phe, thus breaking the H-bond to a specific ec3 cofactor. We find that the rate of primary charge separation (CS) is lowered in both mutants, providing direct evidence that the primary ET event can be initiated independently in each branch. Furthermore, the data provide further support for the previously published model in which the initial CS event occurs within an ec2/ec3 pair, generating a primary ec2 þ ec3 − radical pair, followed by rapid reduction by P 700 in the second ET step. A unique kinetic modeling approach allows estimation of the individual ET rates within the two cofactor branches.Chlamydomonas | electron transfer directionality | femtosecond absorption | photosystem I | ultrafast spectroscopy I n oxygenic photosynthesis, the primary reactions of light utilization are driven by two multisubunit, pigment-protein complexes-photosystem II (PSII) and photosystem I (PSI) (1-3). The structures of PSI from the cyanobacterium Thermosynechococcus elongatus (4) and from the plant Pisum sativum (5) have been resolved to 2.5 Å and 3.4 Å, respectively. The PSI core complex consists of an extensive antenna (ANT) system of ∼100 densely packed Chls and a relatively isolated group of redox (reduction-oxidation reaction) active cofactors at the center composing the reaction center (RC). As in all other RCs, the cofactors in the RC of PSI form two quasi-symmetric branches (Fig. 1), diverging from a Chl a 0 ∕Chl a pair (ec1 A ∕ec1 B ) traditionally called P 700 (4). In each branch is a pair of Chl a molecules (ec2 A ∕ec3 A or ec2 B ∕ec3 B ) and a phylloquinone (PhQ A or PhQ B ). Finally, the branches join again at the F X iron-sulfur (FeS) cluster.The symmetry of the cofactor branches is key to discussion of the directionality of electron transfer (ET) in PSI. Originally, it had been assumed that, analogous to the type II RCs, ET in PSI proceeded along only one of the cofactor branches, and that the other branch was not used. This idea would have been supported by the structural asymmetry of P 700 , if P 700 were the primary electron donor in PSI. However, evidence was provided that muta...

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“…Site-directed mutations of the Met serving as axial ligand to each ec3 Chl have been described in Chlamydomonas (6)(7)(8) and Synechocystis (9,10). Ultrafast pump-probe data from the C. reinhardtii mutants indicate a slowing or blockage of ET from the affected ec3 Chl in mutants of both PsaA-Met-688 § § and PsaB-Met-668 (8); along with pulsed EPR data from the same mutants (7,12), these data implied the use of both branches. In contrast, experiments with the Synechocystis mutants implied that ET is strongly biased toward the A-branch.…”

mentioning

confidence: 98%

Directing electron transfer within Photosystem I by breaking H-bonds in the cofactor branches

Est

Lucas

et al. 2006

Proc. Natl. Acad. Sci. U.S.A.

101

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Photosystem I has two branches of cofactors down which lightdriven electron transfer (ET) could potentially proceed, each consisting of a pair of chlorophylls (Chls) and a phylloquinone (PhQ). Forward ET from PhQ to the next ET cofactor (F X) is described by two kinetic components with decay times of Ϸ20 and Ϸ200 ns, which have been proposed to represent ET from PhQ B and PhQA, respectively. Immediately preceding each quinone is a Chl (ec3), which receives a H-bond from a nearby tyrosine. To decrease the reduction potential of each of these Chls, and thus modify the relative yield of ET within the targeted branch, this H-bond was removed by conversion of each Tyr to Phe in the green alga Chlamydomonas reinhardtii. Together, transient optical absorption spectroscopy performed in vivo and transient electron paramagnetic resonance data from thylakoid membranes showed that the mutations affect the relative amplitudes, but not the lifetimes, of the two kinetic components representing ET from PhQ to F X. The mutation near ec3 A increases the fraction of the faster component at the expense of the slower component, with the opposite effect seen in the ec3B mutant. We interpret this result as a decrease in the relative use of the targeted branch. This finding suggests that in Photosystem I, unlike type II reaction centers, the relative efficiency of the two branches is extremely sensitive to the energetics of the embedded redox cofactors.Chlamydomonas ͉ directionality ͉ photosynthetic reaction center ͉ pump-probe spectroscopy ͉ transient EPR P hotosynthetic reaction centers (RCs) are the membrane proteins responsible for the capture and storage of light energy in photosynthetic organisms. As with all of the RCs, Photosystem I (PS1) has a C2 symmetrical structure with two virtually identical branches of redox cofactors extending across the membrane (see Fig. 1). The x-ray crystal structure of PS1 from Thermosynechococcus elongatus (1) has allowed identification of amino acid residues interacting with the electron transfer (ET) cofactors, permitting the use of site-directed mutagenesis to investigate to what extent ET occurs in the two branches. Many of these studies (2-10) point toward the possibility that ET takes place in both branches of cofactors (A-branch and Bbranch; see Fig. 1). The data consistently show that the major fraction occurs in the A-branch and that the slow phase of ET from phylloquinone (PhQ) to F x is associated with this branch. The involvement of the B-branch is less clear, but there is mounting evidence to support the assignment of the fast component of PhQ to F x ET to this branch. If ET does indeed occur in both branches in PS1, this behavior would be remarkably different from the type II RCs. In purple bacterial RCs, for example, it is well known that initial ET is biased almost exclusively toward the A-branch, probably because the B-branch quinone is a mobile electron and proton carrier in this type of RC. The strong biasing of the ET in the type II RCs makes it difficult to investigate the fac...

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Bidirectional Electron Transfer in Photosystem I: Determination of Two Distances between P₇₀₀⁺ and A₁^- in Spin-Correlated Radical Pairs

Cited by 89 publications

References 48 publications

Alteration of the Axial Met Ligand to Electron Acceptor A0 in Photosystem I: Effect on the Generation of P 700 ·+ A 1 ·− Radical Pairs as Studied by W-band Transient EPR

Alteration of the Axial Met Ligand to Electron Acceptor A0 in Photosystem I: Effect on the Generation of P 700 ·+ A 1 ·− Radical Pairs as Studied by W-band Transient EPR

Independent initiation of primary electron transfer in the two branches of the photosystem I reaction center

Directing electron transfer within Photosystem I by breaking H-bonds in the cofactor branches

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