Photosystem II

Abstract

Photosystem II (PSII) is a specialized protein complex that uses light energy to drive the transfer of electrons from water to plastoquinone, resulting in the production of oxygen and the release of reduced plastoquinone into the photosynthetic membrane. The key components of the PSII complex include a peripheral antenna system that employs chlorophyll and other pigment molecules to absorb light, a reaction centre at the core of the complex that is the site of the initial electron transfer reactions, an Mn4OxCa cluster that catalyses water oxidation and a binding pocket for the reduction of plastoquinone. PSII is the sole source of oxygen production in all oxygenic photosynthetic organisms, which include plants, algae and cyanobacteria. In these organisms, PSII operates in series with other protein complexes, including the PSI reaction centre, to produce the reduced form of nicotenamide–adenine dinucleotide phosphate (NADPH) and adenosine triphosphate (ATP), which is used in the Calvin–Benson cycle to produce carbohydrates from carbon dioxide.

Key concepts

  • Photosystem II (PSII) is a membrane‐embedded protein–pigment complex, containing more than 20 subunits and approximately 100 cofactors.

  • Antenna and reaction centre regions in PSII are in separate protein complexes.

  • Light is absorbed by chlorophyll, carotenoid and phycobilin pigments in the antenna regions and the excitation energy is rapidly transferred to the reaction centre domain.

  • PSII can switch among different modes to either utilize up to 90% of the incident light for charge separation (under low light conditions) or convert a large portion of the excess light into heat and light (fluorescence) (under high light conditions).

  • The initial light‐induced charge separation results in the formation of a chlorophyll cation and a pheophytin anion which are approximately 10 Å apart; this charge separation is rapidly stabilized by transfer of the charges to other more distant cofactors.

  • The oxidation of water occurs at an Mn4OxCa cluster embedded in the protein environment of subunits D1 and CP43.

  • To oxidize two molecules of water four oxidizing equivalents must be accumulated in the Mn4OxCa cluster by four consecutive light‐induced charge separation(s).

  • There are several conflicting proposals on the mechanism of water oxidation at the Mn4OxCa cluster in PSII.

  • The electrons and protons extracted from water by PSII are finally used to drive the reduction of NADP+ and the production of ATP, respectively.

Keywords: photosynthesis; reaction centre; primary photochemistry; oxygen evolution; electron transport; chlorophyll

Figure 1.

(a) Schematic representation of protein complexes and cofactors involved in the linear electron transport and the proton transport of photosynthesis in higher plants (for differences with other oxygenic organisms, see later discussion and the text). (b) The Z scheme showing the energetics of oxygenic photosynthetic electron transport. The vertical scale shows the equilibrium midpoint redox potential (Em) of the electron transport components. Approximate electron transfer times are shown for several reactions. Looking at the components from the bottom left of the diagrams: Mn4OxCa (or Mn4), tetranuclear manganese–oxygen–calcium cluster, where x⩾4; Yz, tyrosine‐161 on the D1 protein; P680, primary electron donor of photosystem II; P680*, excited electronic state of P680 (for details, see text and Figure c); Pheo, pheophytin; QA, a tightly bound plastoquinone; QB, a plastoquinone that binds and unbinds from photosystem II; PQ, a pool of mobile plastoquinone molecules; the middle box represents a protein complex containing two molecules of cytochrome b6 (Cyt b6; only one is shown), an iron–sulfur protein (FeS; known as Rieske FeS protein) and a cytochrome f (Cyt f); PC, plastocyanin (cyanobacteria often employ Cyt c6); P700, reaction centre chlorophyll a of photosystem I; P700*, excited electronic state of P700; A0, a special chlorophyll a molecule; A1, vitamin K; FX, FA, FB, iron–sulfur centres; Fd, ferredoxin; FNR, ferredoxin–NADP reductase and NADP+, nicotinamide–adenine dinucleotide phosphate. Figure a shows, in addition, LHC‐I and LHC‐II, light‐harvesting complexes of photosystems I and II, respectively (see Figure b for cyanobacteria), and the ATP synthase with coupling factors (CF0 and CF1). This figure was drawn for the authors by Dmitriy Shevela (in the laboratory of JM).

Figure 2.

(a) Schematic representation of components of photosystem II in higher plants and green algae. (b) Schematic representation of components of photosystem II in cyanobacteria. D1 and D2 are the reaction centre proteins of photosystem II (PSII). PSII uses light energy to remove electrons from water, resulting in the release of oxygen and protons (see the Lumen side of the diagram). The electrons from water are transferred via redox cofactors in the protein complex to form reduced plastoquinone. Mn4OxCa is the manganese–oxygen–calcium cluster involved in removing electrons from water; P680 is a pair of chlorophylls (PD1 and PD2) of PSII; ChlD1 is the primary electron donor and PheoD1, pheophytin on D1, is the primary electron acceptor; QA (on D2), bound plastoquinone; QB (on D1), plastoquinone that binds and unbinds from PSII; Yz (on D1) and YD (on D2) are redox active tyrosine residues in PSII with different functions and PQ, mobile plastoquinone molecules in the membrane. CP43 and CP47 are chlorophyll–protein complexes of 43 and 47 kDa that form the inner (also called core) antenna system of PSII; LHC‐II (light‐harvesting complex II; Figure a) denotes all other PSII antenna in eukaryotes; PsbO (33 kDa), PsbQ (16 kDa) and PsbP (23 kDa) are extrinsic proteins that stabilize and optimize the water‐splitting complex and its reactivity (Figure a); Cyt b559 is a dimeric protein that contains the redox active cytochrome b559 that maybe involved in photoprotection of PSII (this protein is also essential for the assembly of PSII). Bicarbonate (HCO3; hydrogen carbonate) shown in the figure as bound to nonhaeme iron; it may be bound in the form of carbonate (CO32−). In cyanobacteria (Figure b), the major antenna is the phycobilisome that is extrinsic to the membrane and connected to the CP47 protein of PSII via an anchor protein; also, instead of PsbP and PsbQ as extrinsic polypeptides on the luminal side, these organisms have PsbU (12 kDa) and PsbV (Cyt c550) proteins. This figure was drawn by Dmitriy Shevela (in the laboratory of JM).

Figure 3.

Structure of the photosystem II (PSII) complex from the thermophilic cyanobacterium Thermosynechocuus elongatus (Guskov et al., ). (a) A view of one monomer of the complex; the view direction is along the membrane plane. Dimensions, in angstroms, are indicated on the right side. Protein subunits are shown as cartoon and coloured in yellow (D1), orange (D2), red (CP47), magenta (CP43), cyan (Cyt b559), green (PsbO), blue (PsbU), salmon (PsbV) and grey (remaining small subunits). Cofactors are shown as sticks in green (chlorophylls), orange (carotenoids) and blue (haeme). The location of the catalytic site of water oxidation, the Mn4OxCa cluster (x>4), is highlighted at the luminal side. (b) The membrane intrinsic part of PSII; this view is onto the membrane plane from the cytoplasmic side; the colouring is as in panel (a). The reaction centre domain D1 and D2 and the antenna subunits CP43 and CP47 are highlighted by ellipses, and the position of the Cyt b559, the nonhaeme iron (blue sphere) and of QA and QB are labelled. (c) Redox active cofactors in the reaction centre. At the right side, the centre‐to‐centre distances, in angstroms, between the cofactors are indicated starting (from bottom to top) from Ca (yellow sphere) of the Mn4OxCa cluster, to the OH of the tyrosine, labelled as Yz, chlorophyll PD1 (of P680), ChlD1 (green), pheophytin PheoD1 (yellow) and plastoquinone QA (magenta) and the distances between QA, Fe (blue sphere) and QB are given directly in the figure in angstroms. Bicarbonate (more appropriately called hydrogen carbonate) is shown to be bound to the nonhaeme iron. (We do not exclude the possibility that the bound species may also be carbonate). The figure was generated by using the coordinates (pdb code: 3BZ1, 3BZ2) of the 2.9 Å resolution crystal structure. This figure was drawn by one of us (JFK).

Figure 4.

The catalytic site of water oxidation in photosystem II (PSII); amino acids are shown with their 3‐letter codes. (a) Structural model for the metal ions and amino acid ligands of the Mn4OxCa cluster, the redox active tyrosine Yz (Tyr161) and the chlorophyll PD1, as derived from the 2.9 Å resolution crystal structure (Guskov et al., ); the view is along the membrane with lumen at the bottom and cytoplasm at the top. The protein surrounding is shown in cartoon mode in light yellow (D1), orange (D2) and magenta (CP43). Mn (purple), Ca2+ (orange) and Cl (green) ions are shown as spheres, ligating amino acids as sticks. The nitrogen and oxygen atoms of the amino acid ligands are coloured in blue and red, respectively; the carbon atoms are coloured depending on the subunit the amino acid belongs to: yellow for D1, orange for D2 and magenta for CP43. (b) Model for the Mn4OxCa cluster in the dark stable S1 state of the water oxidizing complex, obtained from orientation dependent X‐ray spectroscopy on PSII single crystals (Yano et al., ) embedded in the ligand environment derived from the crystal structure. The colouring and the view direction is as in panel (a), bridging oxygens are shown as small red spheres. (c) Theoretical model for the Mn4OxCa cluster and its first ligand sphere in the S1 state derived from density functional calculations (Siegbahn, ); the colouring and the view direction is as in panel (a); the bridging oxygens are shown as small red spheres. This model also includes some water/hydroxide groups (hydrogens shown in grey) as ligands to the manganese and calcium ions. This figure was drawn by one of us (JFK).

Figure 5.

Schematic representation showing excitation energy transfer (small red arrows) from one chlorophyll molecule to another in a ‘generic’ LHC‐type antenna system of higher plants. Green discs represent chlorophylls a and b, and yellow discs represent carotenoids; the darker green disc in the middle of panel (a) represents an open reaction centre and the lighter green disc in the middle of panel (b) represents a closed reaction centre. When the reaction centre is open (a), most energy is used for charge separation, and the system emits minimal chlorophyll a fluorescence (labelled as F0); when the reaction centre is closed (b), chlorophyll a fluorescence is maximal (Fmax). This figure was drawn by Dmitriy Shevela (in the laboratory of one of us, JM).

Figure 6.

The oxygen cycle (also called the ‘oxygen clock’) of photosystem II (PSII). (a) Oxygen yield from PSII as a function of flash number (oxygen cycle) (see Joliot and Kok, ). (b) One of the current models of the steps in oxygen evolution in PSII. See text and Joliot and Kok for details. (c) Simplified schemes for three currently discussed pathways for the O–O bond formation at the Mn4OxCa cluster in photosystem II. The three displayed mechanisms differ in the way how the substrate ‘water’ molecules (term ‘water’ includes here all deprotonated and partially oxidized water‐derived ligands) are bound, and the O–O bond formation is initiated: (I) via a nucleophilic attack mechanism (S4 is shown); (II) a radical mechanism (S3Yz is shown) or (III) an oxidative coupling of two hydroxo groups within an equilibrium in the S3 state. In the latter example the complexed oxo would represent a minor fraction of the centres, but only this fraction would be oxidized by Yz. For further details see text and the references stated therein. This figure was drawn by Dmitriy Shevela (in the laboratory of one of us, JM).

Figure 7.

The two‐electron gate on the electron acceptor side of photosystem II (PSII). (a) Chlorophyll a fluorescence from PSII, as a function of flash number, after the ‘oxygen cycle’ is inhibited and water is replaced by an artificial electron donor (Velthuys and Amesz, ); data show clearly the two‐flash dependence. (b) Steps in the two‐electron reduction of plastoquinone at the QB site of PSII (see Figure and text for details). This figure was drawn by Dmitriy Shevela (in the laboratory of one of us, JM).

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Further Reading

Björn LO, Papageorgiou GC, Blankenship R and Govindjee (2009) A viewpoint: why chlorophyll a? Photosynthesis Research 99: 85–98.

Blankenship RE (2002) Mechanisms of Photosynthesis. Oxford: Blackwell Science.

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Ke B (2001) Photosynthesis: photobiochemistry and photobiophysics. In: Govindjee (ed.) Advances in Photosynthesis and Respiration, vol. 10. Dordrecht: Kluwer Academic (now Springer).

Lane N (2003) Oxygen – The Molecule That Made the World. Oxford: Oxford University Press.

Morton O (2008) Eating the Sun: How Plants Power the Planet. New York: Harper Collins Publishers.

Rabinowitch E and Govindjee (1969) Photosynthesis. New York: Wiley. Available free at http://www.life.uiuc.edu/govindjee/photosynBook.html.

Van Amerongen H, Valkunas L and Van Grondelle R (2000) Photosynthetic Excitons. Singapore: World Scientific.

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Govindjee, Kern, Jan F, Messinger, Johannes, and Whitmarsh, John(Feb 2010) Photosystem II. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0000669.pub2]