Towards complete cofactor arrangement in the 3.0 Å resolution structure of photosystem II

Abstract

Oxygenic photosynthesis in plants, algae and cyanobacteria is initiated at photosystem II, a homodimeric multisubunit protein-cofactor complex embedded in the thylakoid membrane. Photosystem II captures sunlight and powers the unique photo-induced oxidation of water to atmospheric oxygen. Crystallographic investigations of cyanobacterial photosystem II have provided several medium-resolution structures (3.8 to 3.2 A) that explain the general arrangement of the protein matrix and cofactors, but do not give a full picture of the complex. Here we describe the most complete cyanobacterial photosystem II structure obtained so far, showing locations of and interactions between 20 protein subunits and 77 cofactors per monomer. Assignment of 11 beta-carotenes yields insights into electron and energy transfer and photo-protection mechanisms in the reaction centre and antenna subunits. The high number of 14 integrally bound lipids reflects the structural and functional importance of these molecules for flexibility within and assembly of photosystem II. A lipophilic pathway is proposed for the diffusion of secondary plastoquinone that transfers redox equivalents from photosystem II to the photosynthetic chain. The structure provides information about the Mn4Ca cluster, where oxidation of water takes place. Our study uncovers near-atomic details necessary to understand the processes that convert light to chemical energy.

Photoassembly of the water-oxidizing complex in photosystem II

“…Only within the last three years, has the structural arrangement of each subunit, with respect to each other, been resolved by X-ray crystallography to 3-3.5 Å resolution with considerable certainty (Rfactor = 24 %) [16,17]. PSII isolated from Thermosynechococcus sp.…”

The PSII calcium site revisited

“…If this assignment is correct (see Chu et al 2001), the latest information from X-ray crystallography (Loll et al 2005b) suggests that the bridging carboxylate could be D1 Glu 189 or Ala 344, but neither of these would agree with the FTIR data (Strickler et al 2005(Strickler et al , 2006. Noguchi et al (1995) concluded from the overall suppression of the S 1 to S 2 FTIR changes that Ca 2+ depletion makes this carboxylate dissociate from manganese as well, but since their sample was probably in the S 1 (K + ) state (Kimura and Ono 2001), we would conclude that no S 1 to S 2 transition occurred.…”

“…The most recent example is shown in Fig. 1, taken from Loll et al (2005b). It is now known, that all of the published structures are compromised by radiation damage to the Mn cluster of the OEC.…”

“…Ferreira et al (2004) represented the structure of Ca 2+ as part of a cubane with three Mn atoms, and no protein ligands to the metal were shown. In contrast, Loll et al (2005b) proposes the structure of carboxylate oxo anion ligands to Ca 2+ from Glu189 and Ala 334, both of which provide oxo anion ligands to Mn atoms of the cluster (see Fig. 1), and Yano et al (2006) add oxo anion ligation from Asp 170.…”

“…Murray and Barber (2006) analyzed data in Ferreira et al (2004) and speculate that a Ca 2+ binding site is present in T. elongatus PsbO that is near the lumenal side of PSII. At the same time, all of the currently available models based on crystallographic data (Loll et al 2005b) or on EXAFS results (Yachandra 2005;Yano et al 2006) place the functional Ca 2+ site in the OEC in close proximity to the Mn cluster, and do not predict ligation by amino acid side chain residues of PsbO.…”