Review
Crystal structure of cyanobacterial photosystem II at 3.0 Å resolution: A closer look at the antenna system and the small membrane-intrinsic subunits

https://doi.org/10.1016/j.plaphy.2008.01.003Get rights and content

Abstract

Photosystem II (PSII) is a homodimeric protein-cofactor complex embedded in the thylakoid membrane that catalyses light-driven charge separation accompanied by the water splitting reaction during oxygenic photosynthesis. In the first part of this review, we describe the current state of the crystal structure at 3.0 Å resolution of cyanobacterial PSII from Thermosynechococcus elongatus [B. Loll et al., Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II, Nature 438 (2005) 1040–1044] with emphasis on the core antenna subunits CP43 and CP47 and the small membrane-intrinsic subunits. The second part describes first the general theory of optical spectra and excitation energy transfer and how the parameters of the theory can be obtained from the structural data. Next, structure–function relationships are discussed that were identified from stationary and time-resolved experiments and simulations of optical spectra and energy transfer processes.

Introduction

Solar energy is harnessed by different types of organisms in a process called photosynthesis. The variant carried out by cyanobacteria, some algae (Protista) and higher plants (Plantae) is called oxygenic photosynthesis, since it uses water as the ultimate source of reducing equivalents, thereby producing molecular oxygen. The key reactions, in which light energy is transformed into chemical energy, take place in two multimeric pigment-protein complexes (PPCs) called photosystem I (PSI) and photosystem II (PSII). These photosystems are part of a complex machinery associated with the thylakoid membrane [1].

From the enzymatic point of view, PSII is a membrane-embedded water:plastoquinone oxidoreductase [2], [3]. It contains the site of water-cleavage and utilizes the electrons extracted from water to reduce plastoquinone. The formed plastoquinole diffuses through the thylakoid membrane (quinone pool) until it finds its way to the cytochrome-b6f-complex, another membrane protein [4]. Here, plastoquinole is re-oxidized and the electrons are transferred to a water-soluble electron carrier (plastocyanin or cytochrome c6). This carrier in turn is oxidized by PSI, a membrane-standing plastocyanin:ferredoxin oxidoreductase [5], that delivers the electrons via ferredoxin to the enzymes producing NADPH. During the action of these enzymes, a proton gradient across the thylakoid membrane, termed proton motive force, is build up that is utilized in ATP synthesis [6].

During the last six years, significant progress has been made in elucidating the spatial structures of membrane proteins involved in oxygenic photosynthesis. Besides the structures of PSI of cyanobacteria [7] and higher plants [8], [9], the cytochrome-b6f-complex of cyanobacteria [10] and algae [11], and the major light-harvesting complex LHC-II of higher plants [12], [13], a number of medium resolution crystallographic models of cyanobacterial PSII appeared, ranging from 3.8 to 3.2 Å [14], [15], [16], [17], [18]. Recently, the crystal structure of PSII from Thermosynechococcus elongatus could be improved to 3.0 Å resolution [19]. The latter structural model revealed many novelties concerning the cofactor inventory and uncovered misinterpretations of previous models at lower resolution. Therefore, the present review is based exclusively on this most recent crystal structure (pdb entry 2AXT).

Extensive biochemical characterization of the crystallizing material [20], [21], [22] indicated that the isolated, active PSII occurs as homodimers of core complexes with each monomeric part being composed of about 20 different protein subunits. On the basis of the 3.0 Å resolution structural model, 77 cofactors per monomer could be identified, including 35 chlorophyll a (Chla), two pheophytin a (Pheoa), two plastoquinone, 11 β-carotene, 14 lipids and three detergent molecules [23], two haems, a non-haem iron, a calcium ion, one bicarbonate anion as well as the metal ions of the Mn4Ca-cluster [24], [25]. In addition, the total number of detergent molecules forming a belt around the PSII dimer in aqueous solution was estimated to ∼350 [26].

A common feature of oxygenic and anoxygenic photosynthesis (where the latter is carried out by certain bacteria [27]) is that the chlorophyll (or bacteriochlorophyll) pigments are involved in two distinct types of processes: Excitation energy transfer (EET) and electron transfer (ET). Accordingly, the PPCs can be grouped into two classes: The reaction centres (RCs), which harbour only a small number of specialized pigments performing ET, and the light-harvesting complexes (LHCs) or antenna proteins [28], [29], which contain the vast majority of photosynthetic pigments and deliver the energy of absorbed photons to the RC by performing EET. In this way, the LHCs effectively increase the absorption cross section of the RCs. The activity of the LHCs has to be adapted to supply and demand of photons. In this context, supply means the actual light conditions experienced by the organism, while demand refers to the need for NADPH and ATP reflected by, e.g., the redox state of the quinone pool and the proton motive force [30], [31].

There are several ways of regulating light-harvesting activity. One possibility is non-photochemical quenching. In this process, the efficiency of EET from the antenna to the RCs is influenced by changing the rate of competing non-radiative transitions that lead to a depopulation of excited states in the antenna [32], [33]. The detailed mechanism of non-photochemical quenching is not yet understood and an active field of research. Another possibility is to vary the amount of LHCs relative to RCs by means of changes in gene expression [34], [35], [36] and/or proteolysis [37]. In addition, LHCs may be shifted from one photosystem to the other in a process termed state transition [38], [39]. Finally, one also has to consider the influence of photosystem stoichiometry, i.e. the relative amount of PSI and PSII, on the quantum efficiency of light-energy conversion [39], [40]. It appears to be a common motif of photosynthetic organisms that there is always a minimal amount of antenna pigments associated with the RC in a fixed stoichiometry, forming what is called a fixed photosynthetic unit (FPU). The FPU-pigments are supplemented by those of separate antenna complexes, the amount of which is subject to regulation as described above. Altogether, therefore, the pigments form a variable photosynthetic unit (VPU) [41], [42].

PSI and PSII could be considered as the FPUs of oxygenic photosynthesis, but this terminus is problematic in view of the variable PSI/PSII ratio [39], [40]. Therefore, the photosystems PSI and PSII are referred to as core complexes (PSIcc and PSIIcc). Besides the RC architecture (type I or iron–sulphur type in PSI and type II or pheophytin-quinone type in PSII; for definition, see [43], [44]), the two photosystems differ considerably in the size of the core antenna. Whereas there are about 100 Chla pigments per RC in PSI (96 in the case of T. elongatus [7]), only about one third of this number is bound to PSII (35 in the case of T. elongatus [19]). Another important difference is the separability of the RC and the antenna part. The RC and antenna pigments are bound to different protein subunits in PSII (see below), so that they can (at least in principle) be separated from each other without denaturation or cutting of polypeptide chains [45], [46]. This is not the case for PSI, where the two large subunits PsaA and PsaB bind both the RC and most of the antenna pigments [7].

In the first part of this review, we describe the structure of PSIIcc as it appears to us from X-ray crystallography at 3.0 Å resolution [19]. The focus will be on the two subunits PsbB (CP47) and PsbC (CP43) constituting the core antenna and the small intrinsic subunits connected to it. We believe that due to the high homology of cyanobacterial and plant PSIIcc [47], [48], the data concerning T. elongatus to be presented here are of relevance to PSII in general.

Knowing the spatial arrangement of its components is essential for an understanding of a PPC, but the relationship between structure and spectroscopy cannot be established without structure-based calculations [29], [49], [50], [51], [52], [53], [54], [55]. In the second part of the review, we shall, therefore, first explain basic principles of the theory in a simple way and then describe how the optical absorption spectra and EET processes of PSIIcc can be understood on the basis of the structural data.

Section snippets

Overview

The crystals underlying the 3.0 Å resolution structural model are obtained from a fraction of the PSII preparation from T. elongatus containing dimeric PSIIcc [20], [21], [22]. Fig. 1 shows the overall structure of one PSIIcc-monomer forming the crystallographic asymmetric unit. The monomer can also be considered as biologically functional unit, since it is active in water oxidation [20], [21]. Dimers from re-dissolved crystals are active as well [22]. These results imply that the subunits of

Overview

A prerequisite for a quantitative understanding of the optical spectra and EET processes in PPCs is to know the transition energies of the chromophore array. If we restrict the present treatment of PSIIcc to the spectral region around 670 nm, we can consider each Chla as a two-level system with the electronic ground state S0 and the first excited state S1. Due to its polarization along the N21–N23-axis (see Section 3.2, Fig. 13), which is usually defined as the “Y-axis”, the S0→S1 transition is

Acknowledgements

This work was supported by Deutsche Forschungsgemeinschaft through Sfb 498 (TP C7 to A.Z. and TP A7 to T.R.).

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