Structure-Based Identification of Energy Sinks in Plant Light-Harvesting Complex II

The local S-0 -> S-1 transition energies (site energies) and corresponding excitonic couplings of chlorophyll a (Chla) and b (Chlb) pigments bound to trimeric, major light-harvesting complex II (LHCII) of higher plants are calculated on the basis of the two crystal structures (Liu et al. Nature 2004, 428, 287-292; Standfuss et al. EMBO J. 2005, 24, 919-928) by using a combined quantum chemical/electrostatic method (Muh et al. Proc. Natl. Acad. Sci. U.S.A. 2007, 104, 16862-16867) that has been modified to cover membrane proteins and to account more realistically for the behavior of protonatable groups under the conditions of low-temperature optical spectroscopy. The obtained exciton levels are in reasonable agreement with experimental information (including linear absorption, linear dichroism, circular dichroism, fluorescence spectra of native as well as wild-type-minus-mutant difference absorption spectra of recombinant LHCII) and differ from earlier treatments based on fitted site energies (Novoderezhkin et al. J. Phys. Chem. B 2005, 109, 10493-10504) mainly by assigning a lower energy level to Chla 604 (in the nomenclature of Liu et al.) and Chlb 608 and a higher energy level to Chlb 605 and 609. The energy sink at cyrogenic temperatures is located at Chla 610 in the stromal layer of pigments, but structural changes at elevated temperatures may change the nature of the terminal emitter domain (including Chla 610/611/612). The site energy red-shift of Chla 610 is calculated to be significantly larger on the basis of the crystal structure of Standfuss et al. compared to that of Liu et al. due to conformational differences in the neighborhood of this pigment. A possible conformational change in the vicinity of Chla 604 involving tyrosine 112 and neoxanthin is found to strongly affect the site energy of this Chla and render it an alternative energy sink in the lumenal layer. A detailed, structure-based analysis of electrostatic pigment-protein interactions is performed to identify amino acid residues that are of interest for future mutagenesis experiments with the aim to further characterize the energy sinks, putative "bottleneck" states for excitation energy transfer, and potential sites of nonphotochemical quenching.