Photosystem II core antenna complex

In oxygenic photosynthesis, Photosystem I1 is the antenna/RC supercomplex that carries out light-induced charge separation across the membrane by doubly reducing plastoquinone on the acceptor side, and the water-splitting reactions in the oxygenevolving complex attached to the donor side (Sauer, 1979; Barber and Santini et al., 1994; Kuhlbrandt, 1999). The intermediate-resolution X-ray structures shown in Fig. 2.11 (p. 86) at 3.8 A resolution have recently been reported for the core PSII complex of the cyanobacterium S. elongatus; this occurs in its native form as a homodimer in the membrane (Zouni et al., 2001; Kamiya and Shen, 2003). The monomeric unit of the PSII core complex is made up of at least 21 protein subunits, 18 of them located within the photosynthetic membrane. In contrast to the PSI supercomplex, the RC pigments and the antenna pigments of the PSII core complex are bound to different protein subunits. The RC pigments, 4 Chls and 2 pheophytins are located on the D1 @sbA) and D2 @sbD) subunits (Fig. 2.12, p. 87). These RC subunits are highly homologous to the L and M subunits of the purple bacterial RC complex and to the cofactor positioning.
 

The subunits carrying the antenna pigments are CP43 (PsbC) and CP47 (PsbB), which are arranged around a local pseudo-C2 axis in the monomer. Each has 6 transmembrane helices arranged as a pseudo-trimer. This structure is very similar to the six amino-terminal transmembrane-helices of PsaA and PsaB, the large core subunits in the PSI RC, suggesting that the two types of reaction centre had a
common ancestor.
 

According to the X-ray structures, CP43 and CP47 bind 12 and 14 Chl a molecules respectively. As in the PSI RC complex, the Chl pigments are arranged in two layers close to the two membrane surfaces, most of them presumably being bound via histidine ligands to the protein (Fig. 2.13, p. 88). The range of centre-tocentre distances for the Chls is 8.5-13 A, within the range expected for rapid energy transfer. Compared with the purple bacterial RC, the D1 and D2 subunits each carry one additional Chl, Chl Z ~anId Chl zD2, respectively. These Chls, despite being bound to the RC subunits, are relatively far distant (about 30 A) from the RC pigments. They may act partly as linker Chls in energy transfer to the core RC. The nearest antenna Chls of the CP43 and CP47 subunits are somewhat closer, at a distance of 20 A, but this is still a relatively large distance for energy transfer to the RC.
 

The energy-transfer steps have been studied in isolated CP43 and CP47 complexes, and overall energy trapping in the intact core complex. In the isolated complexes, energy equilibration is very fast, mostly in the time range of 0.2-0.4 ps, with some slower 2-3 ps contributions (de Weerd et al., 2002a and 2002b). The fast transfer steps, which have mainly been assigned to equilibration in the Chl layer near the stromal side of the membrane, imply average single-step transfer times of -100 fs between pairs of Chls. Such fast rates are expected from the relatively close packing of the Chls, and are in reasonable agreement with theoretical calculations (de Weerd et al., 2002b). The slower transfer step has been assigned to transfer from the lumenal to the stromal layer of Chls, and to the transfer to the lowest-energy excitonic state in each system at low temperature. This final transfer step may however be substantially faster at room temperature. De Weerd et al. (2002b) have concluded that the rates of energy transfer within the isolated CP43 and CP47 complexes are fast enough not to limit the overall trapping of excitation energy in Photosystem 11.
 

The initial trapping of energy by charge separation in the RC of PSII core complexes occurs in about 40 ps in cyanobacterial complexes of S. elongatus (Schatz et a/., 1987 and 1988) and increases up to -200-250 ps for the large PSII antenna/RC particles of higher plants (Holzwarth and Roelofs, 1992). From a comparison of the trapping lifetimes and rates with open and closed RCs, it had been concluded before the X-ray structure determination that kinetics in the PSII core are mostly trap-limited (Schatz et al., 1987 and 1988). Since the antenna and the RC are essentially isoenergetic at room temperature, the 40 ps lifetime and the 32 pigments per RC would, according to the simple picture of trapping presented in Section 2.1.2, imply a primary charge-separation rate of about (1.3-1.5 ps)-l within a trap-limited model.
 

However, recent modelling based on the structural data has led to widely deviating conclusions (Vasiliev et al., 2001 and 2002). According to these workers, the fastest transfer steps from the antenna Chls into the RC are slower than 5 ps because of the large antenna-to-RC distances, which may be necessary for avoiding oxidation of the antenna Chls by oxidised P680. They thus advocated a transfer-to-trap-limited model for energy transfer in the PSII core complex, arguing that electron transfer in the RC is much faster than transfer from the antenna to the RC.
 

Many assumptions about unknown spectral properties are involved in such modelling, and as yet it is not clear whether the transfer-to-trap-limited model is correct since there are several unexplained contradictions with other data. For example, it is well known that the fluorescence yield and lifetime of PSII critically depend on whether the RC is open or closed (see, for example, Holzwarth and Roelofs, 1992). This cannot easily be explained within a transfer-to-trap-limited model, but it is easily understood within an essentially trap-limited model (Holzwarth and Roelofs, 1992): if one assumes at the extreme a situation where energy equilibration between antenna and RC occurs at about the same rate as charge separation in the RC, one would still have an essentially trap-limited model which would at the same time be consistent with the RC redox-state sensitivity of the fluorescence lifetime and the antenna size dependence of the PSII lifetime. We thus believe that the models of Vassiliev et al. (2002) and Dekker and van Grondelle (2000) are too extreme, and further work is necessary finally to clarify the transfer steps in the PSII core.
 

A recent detailed study of the dependence of trapping kinetics on antenna size in various PSII particles also came to the conclusion that indeed there is a shallow equilibrium established in PSII prior to charge separation (Barter et al., 2001), consistent with the early model and conclusions of Schatz et al. (1988) and Holzwarth and Roelofs (1992). Barter et al. (2001) concluded that a shallow equilibrium between the antenna and reaction centre in Photosystem I1 would facilitate regulation via, for example, non-photochemical quenching, and went on to propose that Photosystem II is optimised for regulation rather than for efficiency. However, the efficiency of PSII in the absence of quenching is very high (usually better than 92%), which implies that regulation capabilities and high efficiency are not in any way mutually exclusive. In conclusion, at present it seems likely that Photosystem I1 kinetics are essentially trap-limited rather than transfer-to-trap-limited.