Substitution of a Chlorophyll into the Inactive Branch Pheophytin-Binding Site Impairs Charge Separation in Photosystem II

Abstract

All photosynthetic reaction centers (RCs) have two parallel sets of electron transfer cofactors that cross the membrane. In quinone-type RCs (including photosystem II (PSII)), however, only one pathway (the active branch) is used for electron transfer. Since the electron transfer cofactors of each pathway have nearly identical distance and orientation relationships, it is assumed that local differences in protein environment determine the directionality of electron transfer. To understand further the factors that affect energy distribution among the PSII RC cofactors, we altered the PSII RC cofactor symmetry by replacing the inactive-branch pheophytin (Pheo) with a chlorophyll (Chl). We mutated the D1-L210 residue to a histidine (D1-L210H) to provide a Mg ligand for Chl. Analyses of the pigment composition of D1-L210H RCs indicated that the inactivebranch Pheo had been replaced by a Chl. Comparisons of wild-type and D1-L210 transient absorption spectra confirmed that the red-shifted Pheo Qx absorption band (543.5 nm) belonged to the active-branch Pheo. Surprisingly, intact D1-L210H PSII complexes were unable to evolve oxygen, lacked Chl variable fluorescence, (following a flash), and were unable to photoaccumulate reduced Qa, indicating that electron transfer in D1-L210H PSII complexes was severely perturbed. The kinetics of primary charge separation, however, were not substantially altered in D1-L210H RCs, indicating that the Chl substitution had not perturbed the energetics of the primary electron donor/acceptor pair. Significantly, intact D1-L210H PSII core complexes had a substantially increased and red-shifted Chl fluorescence emission band attributed to fluorescence from Chl's of the distal antenna complex as well as a blue-shifted fluorescence emission peak attributed to Chl's of the proximal antenna complex (77 K). These results are interpreted in terms of a redistribution of the excitedstate energy among the pigments of the RC multimer, leading to loss of the excited state via fluorescence in the D1-L210H mutant.

Quantum Biological Switch Based on Superradiance Transitions

“…Even though there is no general consensus on the role quantum coherence plays in the electron transfer (ET) efficiency ( 99%) [15][16][17][18][19][20], there is no doubt that the models for exciton transport in the LHCs and primary charge separation in the reaction centers (RCs) should utilize quantum coherent effects.The photosystem II (PSII) RC of many bacteria, plants and algae, where the primary charge separation occurs, is arranged in two symmetric branches, even if only one of them is active for the ET. Different mechanisms which could be responsible for the asymmetry in the ET in the PSII RCs, and the related experiments, are discussed in [21][22][23][24][25][26][27][28][29][30] (see also references therein).Here we do not address the question why only one branch is active, but we use the PSII RC as a prototype for an artificial biological switch, able to drive the ET to the left or the right symmetric branch, by controlling the couplings to the sinks.Primary charge separation in the RC can be modeled starting from a donor (a dimer, called the special pair where the excitation starts) and then including the ET through different protein subunits, (bacterio)chlorophylls and (bacterio)pheophytins, generally called chromophores. This transfer occurs in a very short time (a few picoseconds).…”

Chlorophylls, Symmetry, Chirality, and Photosynthesis

“…The symmetry of their arrangement and similarity to the bacterial center is evident in the crystal structure of the Thermosynechococcus vulcanus oxygen-evolving PS II (Figure 33). The symmetry of the cofactor arrangement is also maintained, as is the unidirectionality of the electron transfer [212]. Likewise the main protein subunits which are involved in the cofactor binding, D1 and D2, are symmetrically related around an approximate two-fold axis of symmetry similar to the bacterial species [196].…”

Picosecond spectroscopy of the isolated reaction centers from the photosystems of oxygenic photosynthesis—ten years (1987–1997) of fun

“…Thereafter the work continued on into the new millennium at Northwestern University with new collaborators (especially Dick Sayre at Ohio State University), a new organism (Chlamydomonas reinhardtii rather than spinach as examined above), and a new emphasis on PS II RC mutants (Wang et al 2002;Xiong et al 2004). …”