Oxygenic photosynthesis forms the basis of aerobic life on earth by converting light energy into biologically useful chemical energy and by splitting water to generate molecular oxygen. The water-splitting and oxygen-evolving reaction is catalyzed by photosystem II (PSII), a huge, multisubunit membrane-protein complex located in the thylakoid membranes of organisms ranging from cyanobacteria to higher plants. The structure of PSII has been analyzed at 1.9-Å resolution by X-ray crystallography, revealing a clear picture of the Mn₄CaO₅ cluster, the catalytic center for water oxidation. This article provides an overview of the overall structure of PSII followed by detailed descriptions of the specific structure of the Mn₄CaO₅ cluster and its surrounding protein environment. Based on the geometric organization of the Mn₄CaO₅ cluster revealed by the crystallographic analysis, in combination with the results of a vast number of experimental studies involving spectroscopic and other techniques as well as various theoretical studies, the article also discusses possible mechanisms for water splitting that are currently under consideration.

Photosystem I enters into the spotlight: Plants rely on large complexes of proteins, chlorophyll, and other cofactors to turn light into chemical energy. Qin et al. present the crystal structures of photosystem I (PSI) and the light-harvesting complex I (LHCI) supercomplex from pea plants (see the Perspective by Croce). The well-resolved structure of the outer antenna complexes and their interaction with the PSI core provide a structural basis for calculating excitation energy transfer efficiency. Moreover, the organization and orientation of chlorophyll and carotenoid cofactors within and between PSI and LHCI hint at energy transfer and photoprotection mechanisms. Science , this issue p. 989 ; see also p. 970

Inspecting S states in photosynthesis: Oxygenic photosynthesis uses a Mn ₄ CaO ₅ cluster in the oxygen-evolving complex to extract electrons from water and produce dioxygen. Visualizing each of the chemical states in this process, S ₀ to S ₄ , and assigning chemical identities and mechanisms on the basis of structures has been a challenge addressed recently by work at x-ray free-electron lasers. Suga et al. used serial crystallography at cryogenic temperatures to trap and determine the structures of several stable states during photosystem II water oxidation (see the Perspective by Britt and Marchiori). Changes around the water cluster already happen in the S ₂ state and set the stage for water insertion that occurs during transition to the S ₃ state. A short 1.9-angstrom distance between the two oxygen atoms in the S ₃ state is consistent with theoretical studies supporting an oxyl/oxo mechanism for oxygen-oxygen coupling. Science , this issue p. 334 ; see also p. 305

All the hues, even the blues: Photosynthetic organisms must balance maximizing productive light absorption and protecting themselves from too much light, which causes damage. Both tasks require pigments—chlorophylls and carotenoids—which absorb light energy and either transfer it to photosystems or disperse it as heat. Wang et al. determined the structure of a fucoxanthin chlorophyll a/c–binding protein (FCP) from a diatom. The structure reveals the arrangement of the specialized photosynthetic pigments in this light-harvesting protein. Fucoxanthin and chlorophyll c absorb the blue-green light that penetrates to deeper water and is not absorbed well by chlorophylls a or b. FCPs are related to the light-harvesting complexes of plants but have more binding sites for carotenoids and fewer for chlorophylls, which may help transfer and disperse light energy. Science , this issue p. eaav0365

The chloride ion, Cl⁻, is an essential cofactor for oxygen evolution of photosystem II (PSII) and is closely associated with the Mn₄Ca cluster. Its detailed location and function have not been identified, however. We substituted Cl⁻with a bromide ion (Br⁻) or an iodide ion (I⁻) in PSII and analyzed the crystal structures of PSII with Br⁻and I⁻substitutions. Substitution of Cl⁻with Br⁻did not inhibit oxygen evolution, whereas substitution of Cl⁻with I⁻completely inhibited oxygen evolution, indicating the efficient replacement of Cl⁻by I⁻. PSII with Br⁻and I⁻substitutions were crystallized, and their structures were analyzed. The results showed that there are 2 anion-binding sites in each PSII monomer; they are located on 2 sides of the Mn₄Ca cluster at equal distances from the metal cluster. Anion-binding site 1 is close to the main chain of D1-Glu-333, and site 2 is close to the main chain of CP43-Glu-354; these 2 residues are coordinated directly with the Mn₄Ca cluster. In addition, site 1 is located in the entrance of a proton exit channel. These results indicate that these 2 Cl⁻anions are required to maintain the coordination structure of the Mn₄Ca cluster as well as the proposed proton channel, thereby keeping the oxygen-evolving complex fully active.

A light-harvesting array in diatoms: Photosynthetic organisms use huge arrays of pigments to draw light energy into the core of photosystem II. The arrangement of these pigments influences how much energy reaches the reaction center. Pi et al. determined the structure of photosystem II from a diatom in complex with an antenna of fucoxanthin–chlorophyll a/c binding proteins (FCPs) (see the Perspective by Büchel). The specialized pigments in this complex allow microalgae to harvest light within a wide range of the visible spectrum. The FCPs are arranged in a pattern analogous to light-harvesting complexes in plants. Science , this issue p. eaax4406 ; see also p. 447