How photosynthetic reaction centers control oxidation power in chlorophyll pairs P680, P700, and P870

Abstract

At the heart of photosynthetic reaction centers (RCs) are pairs of chlorophyll a (Chla), P700 in photosystem I (PSI) and P680 in photosystem II (PSII) of cyanobacteria, algae, or plants, and a pair of bacteriochlorophyll a (BChla), P870 in purple bacterial RCs (PbRCs). These pairs differ greatly in their redox potentials for one-electron oxidation, E m. For P680, Em is 1,100 -1,200 mV, but for P700 and P870, E m is only 500 mV. Calculations with the linearized Poisson-Boltzmann equation reproduce these measured E m differences successfully. Analyzing the origin for these differences, we found as major factors in PSII the unique Mn 4Ca cluster (relative to PSI and PbRC), the position of P680 close to the luminal edge of transmembrane ␣-helix d (relative to PSI), local variations in the cd loop (relative to PbRC), and the intrinsically higher E m of Chla compared with BChla (relative to PbRC).electron transfer ͉ photosystem ͉ redox potential ͉ special pair ͉ electrostatic energy T he essence of photosynthetic reaction centers (RCs) of photosystem I (PSI) and photosystem II (PSII) of cyanobacteria, green algae, and plants, as well as of purple bacterial RCs (PbRCs), are two homologous protein subunits (D1, D2) in PSII, (L, M) in PbRC, and the C-terminal RC domains of subunits (A, B) in PSI. The polypeptide chains of these subunits and the C-terminal domains of PSI are folded into five transmembrane ␣-helices (TMHs) in a semicircular arrangement, and the two subunits in each RC are interlocked in a handshake motif with comparable topography and related by a pseudo-twofold symmetry axis (Fig. 1).We consider here the pair of chlorophyll a (Chla) in PSI (Chla P A/B in P700) and in PSII (Chla P D1/D2 in P680) and the pair of bacteriochlorophyll a (BChla) in PbRC (BChla P L/M in P870), where light-driven charge separation results in positively charged radicals P700 ϩ⅐ , P680 ϩ⅐ , and P870 ϩ⅐ , respectively. In PSI and PbRC, P700 ϩ⅐ and P870 ϩ⅐ are rereduced by small water-soluble proteins. By contrast, P680 ϩ⅐ in PSII is rereduced by a redoxactive tyrosine (D1-Tyr-161, Y Z ), which is subsequently reduced by electron transfer from the unique Mn 4 Ca cluster, where water is oxidized under release of atmospheric oxygen, protons, and electrons. Kinetic studies (1) and computations (2) yielded redox potentials for one-electron oxidation E m (P680) of 1,100-1,300 mV, high enough for P680 ϩ⅐ to act as an electron acceptor for the different Mn 4 Ca redox states. According to recent studies, P680 probably consists of the Chla pair P D1/D2 or the two adjacent accessory Chla, Chl D1/D2 (3).In contrast to PSII, with an unusually high E m (P680) of 1,100-1,300 mV (1, 2), the corresponding E m values in PbRC, E m (P870) ϭ 500 mV (4), and in PSI, E m (P700) ϭ 500 mV (5), are low. Part of these E m differences were associated with electronic coupling, which is weak between Chla in P D1/D2 but strong between Bchla in P L/M because of mutual overlap of BChla rings I. Indeed, in the PbRC mutant His(M202)Leu, where His-202 that coordinates...

α-Helices direct excitation energy flow in the Fenna–Matthews–Olson protein

“…[31][32][33]. Recently, these effects were found to provide an important contribution to pigment redox potentials in photosynthetic reaction centers (20). Here, we have shown that in the FMO protein, the influence of ␣-helices on the formation of an excitation energy funnel is dominant.…”

“…Our simulations take into account all these aspects, allowing us to unravel in detail the various contributions to site energy differences on the basis of a crystal structure. In addition, we consider conformational differences between pigments and the consequences of nonstandard protonation patterns resulting from protein-and environment-induced changes of acid-base equilibria of titratable residues (18)(19)(20). In the classical electrostatic part of the simulations, we calculate the free energy change of the PPC that occurs when the charge density of a pigment in its S 0 state is changed into that of the S 1 state, taking into account the nonequilibrium polarization (21) Author contributions: T.R.…”

Spectroelectrochemical determination of the redox potential of pheophytina, the primary electron acceptor in photosystem II

“…Later, Grabolle and Dau (10) analyzed the delayed and prompt Chl fluorescence of PS II membranes in the absence of inhibitor and assessed the E m (P680/P680 ϩ ) value to be ϩ1.25 V, by citing E m (Q A /Q A Ϫ ) to be Ϫ80 mV. Since then, the value of approximately ϩ1.25 V is generally accepted for E m (P680/P680 ϩ ) (1)(2)(3)(4)(5) and is used as a reference in computational chemistry (13)(14)(15)(16).…”

“…Although the E m (P680/ P680 ϩ ) value is an essential parameter to draw a whole picture of the PS II energetics, its direct measurement has never been attained (10) because water, present as dominant (solvent) molecules in most sample solutions, is oxidized first heavily and tends to mask the subsequent oxidation of the target entity P680 at a higher potential. The E m (P680/P680 ϩ ) value has hence been estimated from the potentials of PS II electron acceptors (10)(11)(12) or assessed by computation (13)(14)(15)(16)(17).…”

The new theory of electron transfer: application to the photosynthetic reaction centre

“…Eq. (6) Due to the wide range of energies and timescales involved [36][37][38][39][40][41], the graph is robust against large measurement errors ( ± 100 mV in potential, ± an order-of-magnitude in lifetime), so we can be confident of the general trend. It is clear that the high energy states are the most short-lived.…”