Proton and electron transfer in the acceptor quinone complex of photosynthetic reaction centers from Rhodobacter Sphaeroides

Abstract

For twenty years the photosynthetic reaction center (RC) has been the premier testing ground for theoretical understanding of electron transfer in aperiodic systems, with special, but not unique, reference to long distance biological electron transport. In addition to the known structure, many of the attributes that make RCs so well suited to studying electron transfer function equally well for any charge movement, including protons. These include the presence of intrinsic reporter groups (electrochromically active pigments), high time resolution through light activation, and a large number and variety of distinct reactions, ranging from loosely coupled responses of the protein dielectric to specific, long distance proton transfers in and out of active sites, and bond making in terminal chemical transformations. A wide variety of biophysical methods have been coupled with site directed mutagenesis to reveal mechanisms of proton uptake, transfer and chemistry in the RC. This review summarizes our progress to date, which suggests that the RC can serve as a paradigm, not only for many energy coupled, membrane proteins, but for the electrostatic and dielectric properties of proteins that are critical to their general function.

Carboxylate Shifts Steer Interquinone Electron Transfer in Photosynthesis

“…Lack of stabilization of an additional charge on Fe(III) due to a different amino acid matrix may explain why the iron in the BRC cannot be oxidized chemically. Q A Ϫ formation results in proton uptake in both reaction centers (18,57), and in PSII, it occurs only after the Q A Ϫ 3 Q B step (57) and likely reflects pK shifts of amino acids in response to Q B Ϫ formation (15,16,18,58). That the kinetic XAS signal was smaller on flash 3 suggests that the shift of BC may not occur in the Q A Ϫ Q B Ϫ state as formed by this flash in preoxidized PSII.…”

“…from its freezing-out at cryogenic temperatures (15,16,59,60) and from the driving force-independent kinetics (15)(16)(17)61). The gating concept explains why the experimentally accessible (monophasic) reaction kinetics are slower than predicted by ET theory (62).…”

“…That the kinetic XAS signal was smaller on flash 3 suggests that the shift of BC may not occur in the Q A Ϫ Q B Ϫ state as formed by this flash in preoxidized PSII. Charge-stabilizing protonation in the vicinity or directly of Q B Ϫ (15,16,58) prior to the second ET (57) may prevent a coordination change of the carboxyl. Studying the coupling between protonation and coordination changes at the Fe is an important direction of future research.…”

“…Crystal structures of PSII so far were reported only at a lower resolution of Ն2.9 Å (7, 8) (a structure at higher resolution may become available in the future) (24). For both PSII and BRCs, in particular the function of the non-heme iron and of its carboxyl ligand in the ET reactions has remained enigmatic (15)(16)(17)(18)(19).…”

“…on the ET kinetics and accompanying protonation reactions (reviewed in Refs. [15][16][17][18][19], preferentially on BRCs for which high resolution (Յ2 Å) crystal data are available (20 -23). Crystal structures of PSII so far were reported only at a lower resolution of Ն2.9 Å (7, 8) (a structure at higher resolution may become available in the future) (24).…”