Charge separation in the reaction center of photosystem II studied as a function of temperature

Groot, Marie Louise; Mourik, Frank van; Eijckelhoff, Camiel; Stokkum, Ivo H. M. van; Dekker, Jan; Grondelle, Rienk van

doi:10.1073/pnas.94.9.4389

Cited by 79 publications

(117 citation statements)

References 45 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The difference in the absorbance spectra of P A and B A poses a fundamental question as to the location and mechanism of primary charge separation in PSII reaction centers. The similarity of the P + Q A --PQ A difference spectrum observed here at 80 K in Synechocystis to that observed at both 5 K (30) and 77 K (54) in Synechococcus indicates that the absorbance spectra of P A and B A are practically invariant between 5 and 80 K and that P + is stabilized on P A at all temperatures including at 5 K. Given the difference in the energies of the lowest excited singlet states (31 meV), the localization of singlet excitation on B A (684 nm) over P A (672.5 nm) is favored by a factor of ∼10 31 at 5 K. As the rate of charge separation is slower (0.4-21 ps) (29,(100)(101)(102) than the rate at which energy is equilibrated within the central pigments of the reaction center (100-250 fs) (103,104), the excited state that drives charge separation must be on B A rather than on P A at low temperature ( Figure 9A,B). This situation is different from what is observed in wild-type bacterial reaction centers where the strong coupling between the P A and P B FIGURE 9: (A) Scheme indicating the various fates of the reaction center following center excitation at 5 and 298 K. The initiators of primary charge separation are B A * at 5 K and B A *, P A * and possibly Ph A * at 298 K. 3 P is stabilized on B A at 5 K but is delocalized at 298 K. P + is stabilized primarily on P A at all temperatures.…”

Section: Location Of 3 P As a Function Of Temperaturementioning

confidence: 99%

“…These authors have speculated that multiple routes for charge separation might exist as well in PSII owing to the much weaker exciton interaction between the reaction center pigments and the absence of a low-energy exciton band of P as a longwavelength trap (33,35). With extrapolation from the bacterial reaction centers, these multiple routes have been proposed by Dekker and van Grondelle (33) as possible sources of the heterogeneity in the kinetics of charge separation that has been observed in PSII (29,(100)(101)(102). Because of the localization of the triplet and the oxidized donor on P in the bacterial reaction centers and the inclined orientation of the reaction center triplet in PSII, Rutherford and co-workers (34,109) have speculated that the monomeric accessory B A chlorophyll might be all or part of P680.…”

Section: Location Of 3 P As a Function Of Temperaturementioning

confidence: 99%

See 1 more Smart Citation

Site-Directed Mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: Sites of Primary Charge Separation and Cation and Triplet Stabilization

et al. 2001

View full text Add to dashboard Cite

Site-directed mutations were introduced to replace D1-His198 and D2-His197 of the D1 and D2 polypeptides, respectively, of the photosystem II (PSII) reaction center of Synechocystis PCC 6803. These residues coordinate chlorophylls P A and P B which are homologous to the special pair Bchlorophylls of the bacterial reaction centers that are coordinated respectively by histidines L-173 and M-200 (202). P A and P B together serve as the primary electron donor, P, in purple bacterial reaction centers. In PS II, the site-directed mutations at D1 His198 affect the P + -P-absorbance difference spectrum. The bleaching maximum in the Soret region (in WT at 433 nm) is blue-shifted by as much as 3 nm. In the D1 His198Gln mutant, a similar displacement to the blue is observed for the bleaching maximum in the Q y region (672.5 nm in WT at 80 K), whereas features attributed to a band shift centered at 681 nm are not altered. In the Y Z •-Y Z -difference spectrum, the band shift of a reaction center chlorophyll centered in WT at 433-434 nm is shifted by 2-3 nm to the blue in the D1-His198Gln mutant. The D1-His198Gln mutation has little effect on the optical difference spectrum, 3 P-1 P, of the reaction center triplet formed by P + Pheo -charge recombination (bleaching at 681-684 nm), measured at 5-80 K, but becomes visible as a pronounced shoulder at 669 nm at temperatures g150 K. Measurements of the kinetics of oxidized donor-Q A -charge recombination and of the reduction of P + by redox active tyrosine, Y Z , indicate that the reduction potential of the redox couple P + /P can be appreciably modulated both positively and negatively by ligand replacement at D1-198 but somewhat less so at D2-197. On the basis of these observations and others in the literature, we propose that the monomeric accessory chlorophyll, B A , is a long-wavelength trap located at 684 nm at 5 K. B A * initiates primary charge separation at low temperature, a function that is increasingly shared with P A * in an activated process as the temperature rises. Charge separation from B A * would be potentially very fast and form P A + B A -and/or B A + Pheo -as observed in bacterial reaction centers upon direct excitation of B A ) Proc. Natl. Acad Sci. 96, 2054-2059. The cation, generated upon primary charge separation in PSII, is stabilized at all temperatures primarily on P A , the absorbance spectrum of which is displaced to the blue by the mutations. In WT, the cation is proposed to be shared to a minor extent (∼20%) with P B , the contribution of which can be modulated up or down by mutation. The band shift at 681 nm, observed in the P + -P difference spectrum, is attributed to an electrochromic effect of P A + on neighboring B A . Because of its low-energy singlet and therefore triplet state, the reaction center triplet state is stabilized on B A at e80 K but can be shared with P A at >80 K in a thermally activated process.

show abstract

Section: Location Of 3 P As a Function Of Temperaturementioning

confidence: 99%

Section: Location Of 3 P As a Function Of Temperaturementioning

confidence: 99%

Site-Directed Mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: Sites of Primary Charge Separation and Cation and Triplet Stabilization

et al. 2001

View full text Add to dashboard Cite

show abstract

“…These dynamics all seem to represent a mixture of energy transfer, excited state decay, radical pair-formation and relaxation, in part due to the shallow equilibria between the excited pigments and the initial radical pair state(s). These observations and the difficulty in identifying the intrinsic charge separation rate (7,(10)(11)(12)(13)(14)(15)(16)(17)(18) undoubtedly reflect the fact that the kinetics in the PSII RC are intrinsically complicated, but in part they are due to the difficulty in disentangling contributions from energy and electron transfer, because of the extensively overlapping pigment absorption bands in the PSII RC combined with the intrinsic heterogeneity of biological systems.…”

mentioning

confidence: 99%

“…Electron transport stops at the H molecule because the final quinone acceptors are missing in these preparations. In contrast to the bacterial RC, in the PSII RC the initial dynamics are highly multiexponential with lifetimes in the order of 100 and 300-400 fs, and 3, 10, and 30 ps (7,(10)(11)(12)(13)(14)(15)(16)(17)(18). These dynamics all seem to represent a mixture of energy transfer, excited state decay, radical pair-formation and relaxation, in part due to the shallow equilibria between the excited pigments and the initial radical pair state(s).…”

mentioning

confidence: 99%

Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy

Groot

Pawlowicz

Wilderen

et al. 2005

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

Self Cite

203

258

View full text Add to dashboard Cite

Despite the apparent similarity between the plant Photosystem II reaction center (RC) and its purple bacterial counterpart, we show in this work that the mechanism of charge separation is very different for the two photosynthetic RCs. By using femtosecond visible-pump-mid-infrared probe spectroscopy in the region of the chlorophyll ester and keto modes, between 1,775 and 1,585 cm ؊1 , with 150-fs time resolution, we show that the reduction of pheophytin occurs on a 0.6-to 0.8-ps time scale, whereas P ؉ , the precursor state for water oxidation, is formed after Ϸ6 ps. We conclude therefore that in the Photosystem II RC the primary charge separation occurs between the ''accessory chlorophyll'' ChlD1 and the pheophytin on the so-called active branch.electron transfer ͉ photosynthesis ͉ pump-probe T he primary steps of energy and electron transfer in green plants' photosynthesis occur in two large protein complexes called Photosystem I and Photosystem II (PSII). PSII is an aggregate of many individual pigment-protein complexes. The core of PSII consists of the chlorophyll (Chl)-binding antennaproteins CP43 and CP47, which feed excitation energy into the D 1 D 2 cytb559 reaction center (RC). Crystal structures of PSII cores from cyanobacteria have been resolved with increasingly high resolution (1-3); currently, the resolution is 3.2 Å (4). The structure of the PSII RC shows four Chls and two pheophytins (H) arranged in two branches very similar to the bacterial RC. In the heart of the PSII RC, there is a dimer of Chls, and in each branch there is one monomeric Chl and one H. Furthermore, there are two distant Chls bound to the periphery of the PSII RC. Although the structure suggests there may be a ''special pair'' of strongly electronically coupled pigments in the PSII RC, the visible absorption spectrum does not show a distinct band. This finding is in contrast to the bacterial RC, where the lowest energy absorption band fully originates from one of the exciton transitions of a special pair of bacteriochlorophylls.Since the first purification of the PSII RC in 1987 (5), it has been speculated that its way of operation would be similar to that of the bacterial RC, with a special pair that upon excitation drives a charge separation in Ϸ3 ps. This idea was based on the strong homology between the bacterial RC and the PSII RC, the strong similarity in the pigment composition, even details in the way the pigments interacted with the protein, and the near-identity of the electron transfer events at the acceptor side. Conversely, it was clear that major differences between the two RCs had to exist at the electron donor side where in the PSII RC charge separation eventually leads to the oxidation of water and the production of molecular oxygen, requiring a very large oxidation potential of the primary electron donor (Ͼ1.2 V vs. 0.45 V in the bacterial RC).In the mid-1990s, it was recognized that energy transfer and charge separation in the PSII RC most likely proceeded in a manner that is very different from that in the b...

show abstract

“…8 On the basis of this fact, detailed models have been proposed for the RC structure of PS II. 9, 10 Much work has been reported on the spectroscopy of the RC, 3,[11][12][13] but little is known about that of CP47. This protein, proximate to the RC, is the last one to be separated from the RC during isolation.…”

Section: Introductionmentioning

confidence: 99%

Spectral Distributions of “Trap” Pigments in the RC, CP47, and CP47−RC Complexes of Photosystem II at Low Temperature: A Fluorescence Line-Narrowing and Hole-Burning Study

et al. 1998

View full text Add to dashboard Cite

Broad-band absorption and fluorescence, fluorescence line-narrowing (FLN), and spectral hole-burning experiments have been performed on the Q y -band of three subcore reaction-center complexes of photosystem II between 1.2 and 4.2 K: the isolated reaction center (RC), the inner core antenna CP47, and the CP47-RC complex. In the RC, fluorescence line-narrowing (FLN) is observed for excitation wavelengths λ exc g 676 nm, whereas in CP47, this occurs for λ exc g 680 nm. The FLN spectra of CP47-RC appear to be the sum of the individual spectra of the RC and CP47, an indication that this complex has two "traps". This has been confirmed from the spectral distributions obtained by measuring the hole depth (at constant hole width) as a function of λ exc , as previously done for the RC [Groot, M. L., et al. J. Phys. Chem. 100, 1996, 11488]. The maxima of these distributions are at ∼682 nm for the RC "trap" and at ∼690 nm for the CP47 "trap" within the CP47-RC complex. Further support that the two distributions of pigments in CP47-RC belong indeed to "trap" pigments is provided by the "effective" homogeneous line width Γ′ hom determined as a function of temperature for various excitation and detection wavelengths.

show abstract

Charge separation in the reaction center of photosystem II studied as a function of temperature

Cited by 79 publications

References 45 publications

Site-Directed Mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: Sites of Primary Charge Separation and Cation and Triplet Stabilization

Site-Directed Mutations at D1-His198 and D2-His197 of Photosystem II in Synechocystis PCC 6803: Sites of Primary Charge Separation and Cation and Triplet Stabilization

Initial electron donor and acceptor in isolated Photosystem II reaction centers identified with femtosecond mid-IR spectroscopy

Spectral Distributions of “Trap” Pigments in the RC, CP47, and CP47−RC Complexes of Photosystem II at Low Temperature: A Fluorescence Line-Narrowing and Hole-Burning Study

Contact Info

Product

Resources

About