Pathways and Timescales of Primary Charge Separation in the Photosystem II Reaction Center as Revealed by a Simultaneous Fit of Time-Resolved Fluorescence and Transient Absorption

Abstract

We model the dynamics of energy transfer and primary charge separation in isolated photosystem II (PSII) reaction centers. Different exciton models with specific site energies of the six core pigments and two peripheral chlorophylls (Chls) in combination with different charge transfer schemes have been compared using a simultaneous fit of the absorption, linear dichroism, circular dichroism, steady-state fluorescence, transient absorption upon different excitation wavelengths, and time-resolved fluorescence. To obtain a quantitative fit of the data we use the modified Redfield theory, with the experimental spectral density including coupling to low-frequency phonons and 48 high-frequency vibrations. The best fit has been obtained with a model implying that the final charge separation occurs via an intermediate state with charge separation within the special pair (RP(1)). This state is weakly dipole-allowed, due to mixing with the exciton states, and can be populated directly or via 100-fs energy transfer from the core-pigments. The RP(1) and next two radical pairs with the electron transfer to the accessory Chl (RP(2)) and to the pheophytin (RP(3)) are characterized by increased electron-phonon coupling and energetic disorder. In the RP(3) state, the hole is delocalized within the special pair, with a predominant localization at the inactive-branch Chl. The intrinsic time constants of electron transfer between the three radical pairs vary from subpicoseconds to several picoseconds (depending on the realization of the disorder). The equilibration between RP(1) and RP(2) is reached within 5 ps at room temperature. During the 5-100-ps period the equilibrated core pigments and radical pairs RP(1) and RP(2) are slowly populated from peripheral chlorophylls and depopulated due to the formation of the third radical pair, RP(3). The effective time constant of the RP(3) formation is 7.5 ps. The calculated dynamics of the pheophytin absorption at 545 nm displays an instantaneous bleach (30% of the total amplitude) followed by a slow increase of the bleaching amplitude with time constants of 15 and 12 ps for blue (662 nm) and red (695 nm) excitation, respectively.

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

“…Or, alternatively, the 1,670-cm Ϫ1 response may be due to Chl D1 (see above) and that at 1,681 cm Ϫ1 may be due to H D1. We can compare this tentative assignment of the PC-P*͞P spectrum, which would indicate that the PC excited state is delocalized over P D1 , Chl D1 , and H D1 , with recent exciton calculations on the pigments in the PS2 RC: Novoderezhkin et al (46) reported the lowest exciton state at Ϸ680 nm to be delocalized mainly over P D1 and Chl D1 , and over H D1 and Chl ZD1 , i.e., the pigments on the active branch of the RC, and charge separation from this state to be very fast, which is in good agreement with our assignments. However, the prediction of the calculations of Raszewski et al (47) is that the lowest exciton states are localized on Chl D1 and H D2 , and the interpretation of P ϩ ͞P spectra of mutants of PS2 cores is that Chl D1 , Chl D2 , H D1 , and H D2 all absorb between 680 and 684 nm but that P D1 and P D2 absorb near 673 and 675 nm, respectively (9,22).…”

Two Different Charge Separation Pathways in Photosystem II

“…-formation, present in the Q x and anion bands, was predicted by the model (19,40) via the (P D1 P D2 Chl D1 Phe D1 )* f…”

Photosynthetic Energy Transfer and Charge Separation in Higher Plants

“…The nonlinear spectral responses can also be expressed in terms of the line-broadening functions (Eq. 3.4), as shown for pump-probe spectra [29,[38][39][40][41][42], Stark spectra [28], photon echoes [36], and 2D echoes [43].…”

“…That model was later replaced by more realistic models based on modified Redfield theory. These models employed the site energies extracted from a simultaneous evolutionarybased fit of linear spectra (OD, CD, LD, and FL) over a wide temperature range [41] and nonlinear spectra (time-resolved OD and FL at room temperature) [39]. In a later work, a CT state, which was strongly mixed with the exciton states, was included in the excitonic manifold [28].…”