Excitation Dynamics in the LHCII Complex of Higher Plants:  Modeling Based on the 2.72 Å Crystal Structure

Abstract

We have modeled steady-state spectra and energy-transfer dynamics in the peripheral plant light-harvesting complex LHCII using new structural data. The dynamics of the chlorophyll (Chl) b-->Chl a transfer and decay of selectively excited "bottleneck" Chl a and b states have been studied by femtosecond pump-probe spectroscopy. We propose an exciton model of the LHCII trimer (with specific site energies) which allows a simultaneous quantitative fit of the absorption, linear-dichroism, steady-state fluorescence spectra, and transient absorption kinetics upon excitation at different wavelengths. In the modeling we use the experimental exciton-phonon spectral density and modified Redfield theory. We have found that fast b-->a transfer is determined by a good connection of the Chls b to strongly coupled Chl a clusters, i.e., a610-a611-a612 trimer and a602-a603 and a613-a614 dimers. Long-lived components of the energy-transfer kinetics are determined by a quick population of red-shifted Chl b605 and blue-shifted Chl a604 followed by a very slow (3 ps for b605 and 12 ps for a604) flow of energy from these monomeric bottleneck sites to the Chl a clusters. The dynamics within the Chl a region is determined by fast (with time constants down to sub-100 fs) exciton relaxation within the a610-a611-a612 trimer, slower 200-300 fs relaxation within the a602-a603 and a613-a614 dimers, even slower 300-800 fs migration between these clusters, and very slow transfer from a604 to the quasi-equilibrated a sites. The final equilibrium is characterized by predominant population of the a610-a611-a612 cluster (mostly the a610 site). The location of this cluster on the outer side of the LHCII trimer probably provides a good connection with the other subunits of PSII.

A comparison of the three isoforms of the light-harvesting complex II using transient absorption and time-resolved fluorescence measurements

“…Only a minor fraction of the excitations on the Chls b is transferred with a time constant of a few picoseconds. 'Blue' absorbing Chls b show a faster decay of the initial bleaching signal than the 'red' Chls b (see Figure 4), which may be due to intraband equilibration within a Chl b dimer (see also, Novoderezhkin et al 2004Novoderezhkin et al , 2005.…”

“…Despite the good description of the absorbance, linear dichroism (LD), fluorescence and TA experiments, it should be realized that most of the experimental data were modeled with the atomic model at 3.4 Å resolution obtained by Ku¨hlbrandt et al (1994). However, very recently new atomic models for LHC II were obtained at 2.72 Å resolution by Liu et al (2004) and at 2.5 Å by Standfuss et al (2005) and many of the spectroscopic properties could be satisfactorily modeled (Novoderezhkin et al 2005). The new model shows two additional chlorophylls and furthermore, the identity and orientation of all the chlorophylls (8 Chls a and 6 Chls b) were revealed.…”

Scalable High-Performance Algorithm for the Simulation of Exciton Dynamics. Application to the Light-Harvesting Complex II in the Presence of Resonant Vibrational Modes

“…16,30,31 However, 2d echo-spectra are more susceptible to vibrational modes and reflect both, electronic and vibrational effects. 10 Due to the lack of computational capabilities, energy-transfer in LHC II had been previously calculated only with approximate methods [32][33][34] with non-conclusive results for the transfer timescales. The predictions for the relaxation time differ by more than one order of magnitude 27,32,[35][36][37] from the results of Renger et al 34 Approximate methods work best in specific limits of delocalized (Redfield type) or incoherent dynamics (Förster transfer), or alternatively try to interpolate between the two cases.…”

“…10 Due to the lack of computational capabilities, energy-transfer in LHC II had been previously calculated only with approximate methods [32][33][34] with non-conclusive results for the transfer timescales. The predictions for the relaxation time differ by more than one order of magnitude 27,32,[35][36][37] from the results of Renger et al 34 Approximate methods work best in specific limits of delocalized (Redfield type) or incoherent dynamics (Förster transfer), or alternatively try to interpolate between the two cases. Any interpolation and combination of Förster/Redfield methods requires to introduce an empirical cut-off parameter, which depends on the precise system parameters (excitonic energies) as well as on the environment (temperature).…”

Excitation Decay Pathways of Lhca Proteins: A Time-Resolved Fluorescence Study

“…The structure of the main peripheral light-harvesting complex of PSII, LHCII, is known with 2.72 Å resolution, 7 and its spectroscopic properties and excitation dynamics are characterized in detail. [8][9][10] Despite the similar pigment arrangement, some of the spectroscopic properties among Lhca proteins and between Lhca and Lhcb proteins are significantly different. The most obvious differences between the Lhca and Lhcb proteins appear in the low-temperature emission spectra, where Lhca proteins show a considerably red-shifted emission compared with that of the Lhcb proteins.…”