Photosynthetic generation of oxygen

Abstract

The oxygen in the atmosphere is derived from light-driven oxidation of water at a catalytic centre contained within a multi-subunit enzyme known as photosystem II (PSII). PSII is located in the photosynthetic membranes of plants, algae and cyanobacteria and its oxygen-evolving centre (OEC) consists of four manganese ions and a calcium ion surrounded by a highly conserved protein environment. Recently, the structure of PSII was elucidated by X-ray crystallography thus revealing details of the molecular architecture of the OEC. This structural information, coupled with an extensive knowledge base derived from a wide range of biophysical, biochemical and molecular biological studies, has provided a framework for understanding the chemistry of photosynthetic oxygen generation as well as opening up debate about its evolutionary origin.

Figure 1

The water-splitting site of PSII showing the Mn₄Ca²⁺ cluster positioned within the Mn anomalous difference map of Ferreira et al. (2004). (a) Based on the model of Ferreira et al. (2004). (b) Schematic of the amino acid ligation pattern for model in (a) with distance less than 3 Å shown by connecting lines. (c) Remodelling the water-splitting site using the native electron density maps of Ferreira et al. (2004) and Loll et al. (2005) and Mn anomalous difference map of Ferreira et al. (2004), keeping the Mn₃Ca²⁺O₄ cubane of Ferreira et al. but with Mn₄ linked to it via a single 3.3 Å mono-μ-oxo bridge (taken from Barber & Murray 2008). (d) Schematic of the amino acid ligation pattern for model in (c) with distance less than 3 Å shown by connecting lines. The Mn anomalous difference map is shown in red and contoured at 5 σ with the fitting of the metal ions into this density by real-space refinement using the molecular graphics programme, Coot (Emsley & Cowtan 2004). The arrow indicates the direction of the normal to the membrane plane.

Figure 2

(a,b) Possible mechanisms for the formation of dioxygen during the S4–S0 transition.

Figure 3

Comparison of the electron transfer cofactors in the (a) reaction centres of photosynthetic purple bacteria (from Rhodopseudomonas viridis; Deisenhofer et al. 1985) and (b) photosystem II (from T. elongatus; Ferreira et al. 2004) emphasizing the similarity on the electron acceptor side for both systems but not on the donor side. The red arrows show the electron transfer pathways. Haem is one of the four haems of the cytochrome donor; BChl and Chl are bacteriochlorophyll and chlorophyll, respectively; BPheo and Pheo are bacteriopheophytin and pheophytin, respectively; L and M refer to L and M subunits, respectively; D1 and D2 refer to D1 and D2 proteins, respectively; MQ, menoquinone; UQ, ubiquinone; PQ, plastoquinone; Fe, non-haem iron. TyrZ and TyrD are redox active D1Tyr161 and D2Try160, respectively.

Figure 4

Comparison of structures (side views) of the (a) RC of purple photosynthetic bacteria (from Rhodopseudomonas viridis; Deisenhofer et al. 1985), (b) the D1 and D2 proteins (from T. elongatus; Ferreira et al. 2004) and (c) PSII monomer core with its 19 different subunits (from T. elongatus; Ferreira et al. 2004).

Figure 5

Overlay of the structures of (a) carbon backbones of CP43 (yellow), CP47 (brown), PsaA (green) and PsaB (blue) and of (b) the conserved 12 Chls of CP43 (yellow), CP47 (purple), PsaA (green) and PsaB based on the crystal structures of PSII (Ferreira et al. 2004) and PSI (Jordan et al. 2001), where suffix C and N indicate C- and N-terminal domains.

Figure 6

Top stromal views derived from X-ray crystallography of (a) PSII (Ferreira et al. 2004) and (b) PSI (Jordan et al. 2001) to emphasize the similarity in the organization of transmembrane helices of CP43/D1 and CP47/D2 with those of PsaA and PsaB.