Functional asymmetry of photosystem II D1 and D2 peripheral chlorophyll mutants of Chlamydomonas reinhardtii

Abstract

The peripheral accessory chlorophylls (Chls) of the photosystem II (PSII) reaction center (RC) are coordinated by a pair of symmetryrelated histidine residues (D1-H118 and D2-H117). These Chls participate in energy transfer from the proximal antennae complexes (CP43 and CP47) to the RC core chromophores. In addition, one or both of the peripheral Chls are redox-active and participate in a low-quantum-yield electron transfer cycle around PSII. We demonstrate that conservative mutations of the D2-H117 residue result in decreased Chl fluorescence quenching efficiency attributed to reduced accumulation of the peripheral accessory Chl cation, Chl Z ؉ . In contrast, identical symmetry-related mutations at residue D1-H118 had no effect on A mong the photosynthetic organisms, there are two different, quinone-type photosynthetic reaction centers (RCs): the oxygenic type present in chloroplasts and cyanobacteria (photosystem II, PSII) and the nonoxygenic type (bacterial reaction center, BRC) as typified by that in purple-sulfur photosynthetic bacteria (for reviews, see refs. 1 and 2). In 1984, the crystal structure of the Rhodopseudomonas viridis BRC was determined at 3-Å resolution by Deisenhofer et al. (3). It soon was recognized that the L and M polypeptides of the BRC had substantial amino acid sequence similarity with the PSII D1 and D2 proteins, respectively. Early models of the D1 and D2 proteinfolding topologies indicated that the PSII D1 and D2 polypeptides were structurally analogous to the L and M subunits (3-8). These models of the PSII RC polypeptides and their associated cofactors were verified by electron and x-ray diffraction of twoand three-dimensional PSII crystals (9-12). Recently, a 3.8-Å resolution structure of the oxygen-evolving PSII complex from Synechecoccus elongatus was determined (13).The PSII RC has six chlorophylls (Chls), two pheophytins (Pheos), two quinones, and one cytochrome b 559 (Cyt b 559 ) heme (8, 13). Significantly, the PSII RC has two additional Chls, relative to the BRC. Site-directed mutagenesis and spectroscopic studies demonstrated that the additional pair of Chls present in PSII is coordinated by a pair of conserved and C 2 symmetryrelated histidine residues (D1-H118 and D2-H117, Chlamydomonas reinhardtii nomenclature) (14-20). Unlike the four Chls and two Pheos involved in primary charge separation, the additional pair of Chls present in the PSII RC is located on the periphery of D1 and D2 polypeptides.Biophysical evidence for the involvement of the peripheral Chls in energy transfer first was obtained from analysis of P680 oxidation kinetics by Schelvis et al. (14). They observed a Ϸ30-ps P680 oxidation lifetime component, which they attributed to energy transfer from a Chl monomer to P680. Based on a Förster mechanism (21) for energy transfer, they calculated that the distance between the peripheral Chl and P680 was 30 Å, a distance confirmed by the recent PSII crystal structure. A similar distance relationship also was predicted on the basis of Chl fluorescence decay kine...

Kinetics and mechanism of electron transfer in intact photosystem II and in the isolated reaction center: Pheophytin is the primary electron acceptor

“…In an analysis of steady-state absorption spectra, we had assigned the two Chl z absorptions to 668 and 678 nm at low temperature (56). More recent work also indicated the pronounced spectral asymmetry of the two peripheral Chl z (13,57). Thus, the SADS for Chl z found here is in agreement with those data.…”

“…Andrizhiyevskaya et al (11) recently also proposed a model with an Ϸ3-ps charge separation. A somewhat slower charge separation of Ϸ8 ps has been reported by Wasielewski and coworkers (12), whereas more recent data from the same group were interpreted in terms of a 2-to 5-ps charge separation time (13). Substantially shorter charge separation times of 1 ps (14) and 0.4 ps (at 240 K) have been reported by Groot et al (15).…”

Two Different Charge Separation Pathways in Photosystem II

“…The evolution in the Phe D1 anion band at 455 nm is in agreement with the slow phases (20 and 300 ps) of RP formation containing Phe D1 . The slower phases of Phe D1 -formation were previously observed (at room and low temperature) but were interpreted as charge separation limited by slow energy transfer from a red Chl z (18,32,36). We will show (see below) that the Chls z * are not populated upon 680-685 nm excitation, which excludes the possibility that the slow charge separation upon red excitation is caused by the energy transfer from Chls z to the RC core.…”

Light-harvesting and structural organization of Photosystem II: From individual complexes to thylakoid membrane

“…Two other Chls (Chlz D1 and Chlz D2) are probably involved in EET from CP43 and CP47 (see Fig. 2) [51,52]. PsbB and psbC encode for the two inner antenna complexes known as CP47 and CP43 respectively with the former being located on the side of D2 and the latter adjacent to D1.…”