Towards a structure-based exciton Hamiltonian for the CP29 antenna of photosystem II

Abstract

The exciton Hamiltonian pertaining to the first excited states of chlorophyll (Chl) a and b pigments in the minor light-harvesting complex CP29 of plant photosystem II is determined based on the recent crystal structure at 2.8 Å resolution applying a combined quantum chemical/electrostatic approach as used earlier for the major light-harvesting complex LHCII. Two electrostatic methods for the calculation of the local transition energies (site energies), referred to as the Poisson-Boltzmann/quantum chemical (PBQC) and charge density coupling (CDC) method, which differ in the way the polarizable environment of the pigments is described, are compared and found to yield comparable results, when tested against fits of measured optical spectra (linear absorption, linear dichroism, circular dichroism, and fluorescence). The crystal structure shows a Chl a/b ratio of 2.25, whereas a ratio between 2.25 and 3.0 can be estimated from the simulation of experimental spectra. Thus, it is possible that up to one Chl b is lost in CP29 samples. The lowest site energy is found to be located at Chl a604 close to neoxanthin. This assignment is confirmed by the simulation of wild-type-minus-mutant difference spectra of reconstituted CP29, where a tyrosine residue next to Chl a604 is modified in the mutant. Nonetheless, the terminal emitter domain (TED), i.e. the pigments contributing mostly to the lowest exciton state, is found at the Chl a611-a612-a615 trimer due to strong excitonic coupling between these pigments, with the largest contributions from Chls a611 and a612. A major difference between CP29 and LHCII is that Chl a610 is not the energy sink in CP29, which is presumably to a large extent due to the replacement of a lysine residue with alanine close to the TED.

Excitation dynamics and structural implication of the stress-related complex LHCSR3 from the green alga Chlamydomonas reinhardtii

“…This assumption is based on the very high structural similarities between all the LHCs crystallized so far, which show an almost perfect overlap between most of the pigments in all structures [22,23,42,64]. However, we allowed for differences in the Chls site energies as compared to LHCII, as it is the case in the other LHCs [32,67]. To this end we treated the energies of the different sites as free parameters in the simultaneous fit of absorption (OD), fluorescence emission (FL), circular dichroism (CD) (see Fig.…”

The quest for energy traps in the CP43 antenna of photosystem II

“…[39][40][41] and V mn for all Chls and Chl pairs, which ultimately yields an answer to the second question. Our electrostatic approach to this problem [36][37][38] is approximate, but turned out to give reasonable results, when applied to the Fenna-Matthews-Olson (FMO) protein of green sulfur bacteria [42][43][44][45], photosystem I [46], the antenna system of plant photosystem II [47][48][49], and the BLUF photoreceptor [50]. In the present paper, we apply it to the CP43 core antenna of PSIIcc, updating earlier work [51].…”

“…In the Poisson-Boltzmann/Quantum chemical (PBQC) method [36,37], the site energy shift is given by (with the index I counting the nuclei) for each pigment type that have been published earlier [47]. These calculations are performed as described [47,49] using TAPBS [60] and the different static dielectric constants p ε = 1.5 -2.0 for the protein, ε mem = 2.0 for the membrane slab, and ε solv = 5.0 for the outer medium. As indicated in eq.…”

“…The excitonic couplings between Q Y transitions of Chls in CP43 were calculated on the basis of the Chl coordinates from the three crystal structures [32,34,35] by using the Poisson-TrEsp method described earlier [37,43,46,49,62] employing MEAD [63] with an optical dielectric constant ε opt = 2.0 [64] and transition charges derived from time-dependent density functional theory (TD-DFT) [65] in the TammDancoff approximation [66] with the B3LYP exchange-correlation (XC) functional [67,68] in QChem [69] and rescaling of the dipole strength based on the data of Knox and Spring [70]. The obtained excitonic couplings are listed in the electronic supplementary material (Appendix A), Tables 4 and 5, together with the values obtained by Shibata et al [15] (based on PDB 3ARC using the same method) and are all very similar.…”

“…For this purpose, we update our earlier structurebased calculation of excitonic couplings and site energies [51] by using in addition to the 2.9 Å resolution structure the more recent ones at 1.9 Å [34] and 2.1 Å [35] resolution. The site energies obtained in this way are used as starting values in a refinement fit of experimental linear optical spectra in the framework of a dynamical theory of optical lineshapes [8,48,49,53,54]. As there remain uncertainties concerning the molecular identity of the trap states, we use our computational approach to propose target residues for mutagenesis experiments that might help to remove these uncertainties in the future.…”