Excited-state energy transfer pathways in photosynthetic reaction centers: 5. Oxidized and triplet excited special pairs as energy acceptors

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, P, a pair of strongly interacting bacteriochlorophylls. Using fluorescence upconversion spectroscopy, energy transfer to the special pair can be monitored by observing the decay of 1 B emission and/or the rise of 1 P. We report 1 B decay kinetics following excitation in the H band in reaction centers where the homodimer and heterodimer (M202HL) special pairs are oxidized, P + and D + , respectively, and when the homodimer special pair is in the triplet state, 3 P. In wild type and the M71GL mutant (a carotenoid-less reaction center), the rates of 1 B decay when P + and 3 P are present, (∼260 fs) −1 and (∼235 fs) −1 , respectively, are similar to that for energy transfer to 1 P (∼190 fs) −1 in wild type measured by either the fluorescence decay of 1 B or the rise of 1 P. In contrast to the homodimer special pair in wild type where the energy transfer rates along the two branches are very similar, singlet energy transfer from the monomeric chromophores along the L and M branches to the heterodimer special pair is asymmetric and is slower along the L side. The 1 B decay in wild type is well described by a single rate constant of (∼190 fs) −1 and in M202HL exhibits two components with rate constants (∼780 fs) −1 and (∼250 fs) −1 . In M202HL reaction centers containing D + , 1 B decays with a single rate constant of (∼343 fs) −1 ; hence, the energy transfer rates along the two branches become similar. Thus, while conversion of the special pair homodimer to a heterodimer breaks the symmetry of ultrafast energy transfer along the two branches of chromophores, symmetry can be restored by oxidizing the heterodimer special pair. To our knowledge, this is the first report of such dramatic alteration of energy transfer within a single reaction center protein. These findings bear on the mechanism of energy transfer in the reaction center and may provide insight into the differences in the electronic interactions on the L vs. M sides of the RC that are relevant to unidirectional electron transfer.