Charge Separation and Energy Transfer in the Photosystem II Core Complex Studied by Femtosecond Midinfrared Spectroscopy

Abstract

The core of photosystem II (PSII) of green plants contains the reaction center (RC) proteins D1D2-cytb559 and two core antennas CP43 and CP47. We have used time-resolved visible pump/midinfrared probe spectroscopy in the region between 1600 and 1800 cm(-1) to study the energy transfer and charge separation events within PSII cores. The absorption difference spectra in the region of the keto and ester chlorophyll modes show spectral evolution with time constants of 3 ps, 27 ps, 200 ps, and 2 ns. Comparison of infrared (IR) difference spectra obtained for the isolated antennas CP43 and CP47 and the D1D2-RC with those measured for the PSII core allowed us to identify the features specific for each of the PSII core components. From the presence of the CP43 and CP47 specific features in the spectra up to time delays of 20-30 ps, we conclude that the main part of the energy transfer from the antennas to the RC occurs on this timescale. Direct excitation of the pigments in the RC evolution associated difference spectra to radical pair formation of PD1+PheoD1- on the same timescale as multi-excitation annihilation and excited state equilibration within the antennas CP43 and CP47, which occur within approximately 1-3 ps. The formation of the earlier radical pair ChlD1+PheoD1-, as identified in isolated D1D2 complexes with time-resolved mid-IR spectroscopy is not observed in the current data, probably because of its relatively low concentration. Relaxation of the state PD1+PheoD1-, caused by a drop in free energy, occurs in 200 ps in closed cores. We conclude that the kinetic model proposed earlier for the energy and electron transfer dynamics within the D1D2-RC, plus two slowly energy-transferring antennas C43 and CP47 explain the complex excited state and charge separation dynamics in the PSII core very well. We further show that the time-resolved IR-difference spectrum of PD1+PheoD1- as observed in PSII cores is virtually identical to that observed in the isolated D1D2-RC complex of PSII, demonstrating that the local structure of the primary reactants has remained intact in the isolated D1D2 complex.

Toward understanding molecular mechanisms of light harvesting and charge separation in photosystem II

“…A fit based on a kinetic model suggested that the slower trapping observed in CP47-RC is caused by a shift of the excited states distribution toward the CP47 antenna, and that the intrinsic rate for energy transfer from CP47 to RC does not limit the overall trapping kinetics in the CP47-RC complex. In contrast to these experimental studies recent resolved visible pump/mid-IR probe studies of the plant PSII core complexes (Pawlowicz et al 2007) and structure-based theoretical calculations (Saito et al 2006) are both in agreement with slow energy transfer from CP43/CP47 antenna to the RC.…”

“…Interestingly the ''effective'' rates (Groot et al 2005b;Holzwarth et al 2006b) and photosystem II core particles (c, d), ref. (Holzwarth et al 2006b;Pawlowicz et al 2007). Values of the rate constants are in 1/ns Photosynth Res (2008) 97:75-89 79 for charge separation and recombination determined by kinetic analysis (Fig.…”

Primary light-energy conversion in tetrameric chlorophyll structure of photosystem II and bacterial reaction centers: II. Femto- and picosecond charge separation in PSII D1/D2/Cyt b559 complex

“…This finding has triggered, however, a discussion on the nature of the primary electron donor in PSII RCs (Van Brederode et al 1999;Dekker and van Grondelle 2000). Recently, the data have been presented suggesting that the lowest excited state in the PSII RC was not necessarily localized on the ''special pair'' P680* and could be on Chl D1 * (Prokhorenko and Holzwarth 2000;Diner et al 2001;Diner and Rappaport 2002;Barter et al 2003;Germano et al 2004;Groot et al 2005;Holzwarth et al 2006;Pawlowicz et al 2007;). However, for example, the photon echo data (Prokhorenko and Holzwarth 2000) are mostly based on excitonic calculations including the site energies which are not well defined yet.…”

Network characteristics of individual pigments in cyanobacterial photosystem II core complexes

“…One is a self-dissipation pathway for the every chlorophyll, in which one unit of excitation leaves the network in one nanosecond [20]. The other one, for nodes in the reaction center, is charge separation, which happens in the picoseconds [21]. To solve the technical problem, we add auxiliary, dummy nodes to express the effects of charge separation and self-dissipation.…”

“…This impressive mechanism begins from the EET in PSII that is located on thylakoid membrane of chloroplast in photosynthetic cells [1]. Especially, there are many experiments focusing on relating the structure and EET properties [2,3,4]. Because the chlorophylls in these pigment-protein complexes are arranged in a peculiar pattern, many researchers have studied the overall EET of system with the orientation and distances of pigment in protein environment [5,6].…”