The earth's primary energy conversion of sunlight into biomass is oxygeneic photosynthesis, driven by large protein-cofactor complexes in the plasma membrane of photosynthetic bacteria and in thylakoid membranes within chloroplasts of plants. These complexes, photosystem II and photosystem I, capture light energy and act sequentially to raise the energy of electrons. These electrons are utilized in electron transport chains to generate a proton gradient across the membrane as well as NADPH. The electromotive force of the proton gradient is used by ATP Synthase to synthesize ATP. Together, this ATP and the NADPH provide energy to drive the light-independent Calvin Cycle, which fixes carbon from CO₂ in organic compounds. See Figure 1 for a schematic of this process.

At left is photosystem II complex (PSII) of the cyanobacterium, Thermosynechococcus elongatus (Ferreira, et al., 2004), which exists as a dimer, viewed from a perspective parallel to the membrane. In a plant chloroplast, this orientation would be such that the top of the molecule would be in the chloroplast stroma, the bottom in the thylakoid lumen, with numerous transmembrane helices embedded in the thylakoid membrane. The PSII dimer is 105 Å deep (45 Å is in the membrane), 205 Å long and 110 Å wide. Each of the monomers comprises at least 19 different protein subunits and 50+ embedded cofactors (e.g. chlorophylls, carotenoids, hemes, plastoquinones, pheophytins, lipids). Many of these cofactors serve as a large antennal system that harvests the energy of photons of light and transfers this energy to the core of the reaction center with high effciency. A chlorophyll dimer (P680) in the reaction center contains electrons that are excited by the energy funneled to them. The P680 electrons are passed through an electron transfer chain (ETC), transferred to cytochrome b₆f via a reduced plastoquinone and then to plastocyanin before reducing the P700 chlorophylls of PSI. The reaction cycle is completed by re-reduction of the P680 chlorophylls by electrons derived from splitting H₂O at the oxygen evolving center (OEC), producing molecular oxygen (O₂) and H⁺ ions that are shunted into the cytosol (bacteria) or thylakoid lumen (plant chloroplasts). See Figure 1 for a schematic of this process.

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The D1 and D2 subunits of each monomer form the center of the complex, each comprising five membrane spanning helices. On either side of the D1 / D2 center, are subunits CP43 and CP47,having six transmembrane helices oriented similarly to the N-terminal domains of the PsaA and PsaB subunits of photosystem I (see tutorial on PSI). The 33-kDa protein, or PsbO, contains an eight-stranded beta barrel that stabilizes the conformation of loops of the D1 protein, which provides a majority of the sidechain ligands that embrace the Mn₄CaO₅ cluster of the oxygen evolving center (OEC - see below).

In addition to 19 protein subunits, each monomer contains 36 chlorophylls, 7 carotenoids, 1 Mn₄CaO₅ cluster, 2 hemes , 2 plastoquinones, 2 pheophytins, lipids, as well as other cofactors. The D1 and D2 subunits house the photosynthetic reaction center and the CP43 and CP47 subunits embrace most of the secondary, antennal, light gathering pigments (D1, D2, CP43, CP47 colors shown for only one of the monomers).

More than 2600 water molecules (O's only - hydrogens not shown) are found in a PSII dimer, clustered at the stromal (top) and lumenal (bottom) membrane surfaces. Membrane bound waters serve as ligands for chlorophylls (not shown).

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The heart of the OEC in each monomer is the cubane Mn₄CaO₅ cluster, which is observed to form a distorted chair (in this view, on its side).

Four water molecules (H₂O - H's not shown) are found near the Mn₄CaO₅ cluster. W1 and W2 coordinate Mn4, whereas W3 and W4 are coordinated to Ca. The waters and numerous charged and polar sidechain ligands from subunit D1, as well as two from CP43 (Arg 357 and Glu 354), provide a saturating ligand environment for the Mn₄CaO₅ cluster. The ligation pattern and distorted chair geometry of the cluster, caused by the greater than average distances between O5 and other ions, suggests that O5 may be involved in O=O (O₂) formation as water is split and electrons and H⁺s are released. W2 or W3 may provide the other substrate. O=O bond formation is likely to occur, then, between two of the three oxygens just discussed (O5, W2, W3). A key residue of subunit D1, tyrosine 161 (Y_z), serves to mediate electron transfer from the Mn₄CaO₅ cluster to the reaction center (see below).

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IV. The PSII Reaction Center

The reaction center responsible for transfer of electrons from the lumen to the stromal surface contains the Mn₄CaO₅ cluster, Y_z chlorophylls, pheophytins, plastoquinones, and a non-heme iron (Fe), liganded by a bicarbonate as well as by histidine ligands from both D1 and D2 subunits (not shown).

Light energy captured by antennal cofactors is transferred to P680 chlorophylls, one of which begins the transfer of electrons towards the stromal suface. These electrons are restored by electrons donated by H₂O in the water splitting reactions discussed above. The electron transfer pathway is illustrated beginning with the Mn₄CaO₅ cluster, proceeding through Y_z, chlorophylls, a pheophytin, a plastoquinone, to the final electron acceptor, plastoquinone QB. Once QB is reduced by 2 electrons, it is released by PSII and will be oxidized as it reduces cytochrome b6f (see the cytb6f exhibit).

An extensive hydrogen bonded network, from the Mn₄CaO₅ cluster through Y_z and extending though water molecules and amino acid sidechains, leads away from the reaction center towards the lumen, in a direction opposite to electron transfer toward the stromal surface.

This H-bonded network as well as two others involving chloride ions that may help maintain the coordination environment of the Mn₄CaO₅ cluster and that lie at the network entrances, form likely pathways to carry protons to the lumen as water is split. The latter two networks may also function as inlet channels for water.

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Ferreira KN, Iverson TM, Maghlaoui K, Barber J, Iwata S. (2004). Architecture of the photosynthetic oxygen-evolving center. Science 303(5665):1831-1838.

Umena Y, Kawakami, K, Shen, J-R, Kamiya N. (2011). Crystal structure of oxygen-evolving photosystem II at resolution of 1.9 Å. Nature 473: 55-60.

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