Excited State Energy Transfer Pathways in Photosynthetic Reaction Centers. 4. Asymmetric Energy Transfer in the Heterodimer Mutant

Abstract

In bacterial photosynthetic reaction centers, ultrafast singlet excited state energy transfer occurs from the monomeric bacteriochlorophylls, B, and bacteriopheophytins, H, to the homodimer special pair, a pair of strongly interacting bacteriochlorophylls. In the M202HL mutant, one of the bacteriochlorophylls comprising the special pair is replaced by a bacteriopheophytin, and this is called the heterodimer special pair or D. We report the direct observation of spontaneous fluorescence from 1 B in the heterodimer mutant. In contrast to results for the homodimer special pair where 1 B decays with a rate constant of (160 fs) -1 (King, B. A.; McAnaney, T. B.; de Winter, A.; Boxer, S. G. J. Phys. Chem. B2000, 104, 8895-8902), 1 B decay in M202HL exhibits two components with rate constants (700 fs) -1 and (190 fs) -1 ; these are similar to what we reported earlier for the rise of 1 D spontaneous fluorescence (King, B. A.; Stanley, R. J.; Boxer, S. G. J. Phys. Chem. B 1997, 101, 3644-3648). In the double mutant M202HL/M182HL, where the accessory bacteriochlorophyll on the M side is replaced by a bacteriopheophytin, the absorption bands corresponding to the chromophores in the BL and BM binding sites are quite well resolved, and it is possible to preferentially excite the chromophore on either the L or the M side. Analysis of the rise of 1 D fluorescence in the double mutant supports the earlier assignment of the slower 700 fs energy transfer component to 1 BL f D, while the faster 190 fs energy transfer component is assigned to 1 BM f D. Replacement of bacteriochlorophyll by bacteriopheophytin in the BM binding site does not alter the time constants of the two energy transfer pathways. Excited state energy transfer to D is the same in QA-depleted and QA-reduced reaction centers, suggesting that electron transfer processes that be might sensitive to a charge on Q A, such as 1 BL f BL + HL - , do not compete with relatively slow 1 BL f D energy transfer. The results support earlier findings that singlet energy transfer from the monomeric chromophores along the L and M branches to the heterodimer special pair is asymmetric and is faster along the M side, in contrast to the homodimer special pair in wild type where the energy transfer rates along the two branches are very similar. Thus, conversion of the special pair homodimer to a heterodimer breaks the symmetry of ultrafast energy transfer along the two branches of chromophores. These findings may provide information on differences in the electronic interactions on the L vs M sides of the RC that is relevant to unidirectional electron transfer.