Photosystem II Secondary article John Whitmarsh, University of Illinois, Urbana, Illinois, USA Article Contents Govindjee, University of Illinois, Urbana, Illinois, USA . Introduction . Organization, Composition and Structure Photosystem II is a specialized protein complex that uses light energy to oxidize water, . Light Capture: The Antenna System resulting in the release of molecular oxygen into the atmosphere, and to reduce . Primary Photochemistry: The Reaction Centre plastoquinone, which is released into the hydrophobic core of the photosynthetic . Oxidation of Water: The Source of Molecular Oxygen membrane. All oxygenic photosynthetic organisms, which include plants, algae and some . Reduction of Plastoquinone: The Two-electron Gate bacteria, depend on photosystem II to extract electrons from water that are eventually used . Photosystem II Contributes to a Proton Electrochemical Potential that Drives ATPase to reduce carbon dioxide in the carbon reduction cycle. The complex is composed of a . Downregulation: Energy is Diverted Away from the central reaction centre in which electron transport occurs, and a peripheral antenna system Reaction Centre when there is Excess Light which contains chlorophyll and other pigment molecules that absorb light. Secondary Electron Transfer Reactions in Photosystem II Protect Against Photodamage . Inactive Photosystem II: A Significant Proportion of Introduction Reaction Centres do not Work In Vivo . Fluorescence: Monitoring Photosystem II Activity In Photosynthetic organisms use light energy to produce Vivo organic molecules (Ort and Whitmarsh, 2001). In plants, . Summary algae and some types of bacteria, the photosynthetic process depends on photosystem II, a membrane-bound protein complexthat removes electrons from water and Chloroplasts originated from photosynthetic bacteria transfers them to plastoquinone, a specialized organic invading a nonphotosynthetic cell. In both chloroplasts molecule. Because the removal of electrons from water and bacteria, thylakoid membranes form vesicles that results in the release of molecular oxygen into the atmo- define an inner and outer aqueous space. Light-driven sphere, this photosystem II-dependent process is known as electron transfer through the photosystem II and photo- oxygenic photosynthesis. Photosystem II is the only system I reaction centres provides the energy for creating a protein complexknown to oxidizewater and release proton electrochemical potential across the thylakoid molecular oxygen. A more ancient form of photosynthesis membrane. The energy stored in the proton electrochemi- occurs in some bacteria that are unable to oxidize water cal gradient drives a membrane-bound adenosine tripho- and therefore do not release oxygen. There is fossil sphate (ATP) synthase that produces ATP. Overall, the evidence that photosystem II-containing organisms light-driven electron transport reactions, occurring evolved about three billion years ago and that oxygenic through the thylakoid membrane, provide NADPH and photosynthesis converted the earth’s atmosphere from a ATP for the production of carbohydrates, the final product highly reducing anaerobic state to the oxygen-rich air of oxygenic photosynthesis. surrounding us today (Des Marais, 2000). By releasing Photosystem II uses light energy to drive two chemical oxygen into the atmosphere, photosystem II enabled the reactions: the oxidation of water and the reduction of evolution of cellular respiration and thus profoundly plastoquinone (Govindjee and Coleman, 1990; Nugent, affected the diversity of life. 2001). The primary photochemical reaction of photosys- Oxygenic photosynthesis depends on two reaction tem II results in separating a positive and a negative charge centre protein complexes, photosystem II and photosys- within the reaction centre and is governed by Einstein’s law tem I, which are linked by the cytochrome bf complexand of photochemistry: one absorbed photon drives the small mobile electron carriers (Whitmarsh and Govindjee, transfer of one electron. This means that four photo- 1999) (Figure 1). Photosystem II, the cytochrome bf chemical reactions are needed to remove four electrons complexand photosystem I are embedded in the thylakoid from water, which results in the release of one molecule of membrane and operate in series to transfer electrons from dioxygen and four protons, and in the reduction of two water to nicotinamide–adenine dinucleotide phosphate molecules of plastoquinone: (NADP 1 ). The energy necessary to move electrons from 1 1 1 water to NADP is provided by light, which is captured by 2H2O 1 2PQ 1 4H 1 (4hn)!O2 1 2PQH2 1 4H the photosystem II and photosystem I antenna systems. In plants and algae the thylakoid membranes are located This chapter focuses on the composition, structure and inside chloroplasts, which are subcellular organelles. In operation of photosystem II. For brevity we describe what oxygenic bacteria the thylakoids are located inside the we know without explaining the experimental results that plasma membrane. underlie our knowledge. The references given at the end of ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net 1 Photosystem II P700* 1–3 ps –1.2 Ao 40–200 ps 15–200 ns A1 3–20 ps 200–500 ns P680* Fx 0.5–20 µs Pheo Photosystem I FA, FB FD NADPH –0.4 100–200 ps + 2H Light FNR NADP+ QA Q Cyt b6 200–600 µs B PQPQ 0 PQ Cyt b6 (volts) 1 ms PQPQ m FeS/Cyt f E Photosystem II 5 ms µ PC 0.4 50–100 s P700 20–200 µs Light 50 µs–1.5 ms 2H2O µ 4Mn 200–800 s 2H+ + Tyr O2 + 4H 1.2 20 ns–200 µs P680 Figure 1 The Z scheme showing the pathway of oxygenic photosynthetic electron transport. The vertical scale shows the equilibrium midpoint potential (Em) of the electron transport components. Approximate electron transfer times are shown for several reactions. Mn, tetranuclear manganese cluster; Tyr * tyrosine-161 on D1 protein (Yz); P680, reaction centre chlorophyll a of photosystem II; P680 , excited electronic state of P680; Pheo, pheophytin; QA,a bound plastoquinone; QB, a plastoquinone that binds and unbinds from photosystem II; PQ, a pool of mobile plastoquinone molecules; the brown box is a protein complex containing cytochrome b6 (Cyt b6), iron–sulfur protein (FeS) and cytochrome f (Cyt f); PC, plastocyanin; P700, reaction centre chlorophyll * a of photosystem I; P700 , excited electronic state of P700; Ao, a special chlorophyll a molecule; A1, vitamin K; FX,FA,FB, iron sulfur centres; FD, ferredoxin; FNR, ferredoxin–NADP reductase; NADP 1 , nicotinamide–adenine dinucleotide phosphate. For details see Whitmarsh and Govindjee (1999). the article are an entryway into the vast literature on Light photosystem II that extends back more than half a century. LHC-ΙΙ CP47 CP43 LHC-ΙΙ Fe2+ Q Organization, Composition and Outside QA B Structure Phe PQ PQ Photosystem II is embedded in the thylakoid membrane, P680 Phe PQ with the oxygen-evolving site near the inner aqueous phase PQ and the plastoquinone reduction site near the outer D1 D2 PQ Tyr Mn aqueous phase (Figure 2), an orientation that enables the Mn oxidation–reduction chemistry of the reaction centre to Inside Mn Mn contribute to the proton electrochemical gradient across 2H2O the thylakoid membrane. In chloroplasts, the photosystem O II and photosystem I complexes are distributed in different 2 + regions of the thylakoid membrane. Most of the photo- 4H system II complexes are located in the stacked membranes (grana), whereas the photosystem I complexes are located Figure 2 Schematic drawing of the photosystem II antenna system and reaction centre in the thylakoid membrane. D1 and D2 are the core in the stomal membranes. It is not clear why two reaction proteins of photosystem II reaction centre. Photosystem II uses light energy centres that operate in series are spatially separated in to remove electrons from water, resulting in the release of oxygen and eukaryotic organisms. In prokaryotes, the thylakoid protons. The electrons from water are transferred via redox cofactors in the membranes do not form grana and the photosystem II protein complex to form reduced plastoquinone. (Mn)4, manganese and I complexes appear to be intermixed. In eukaryotes the cluster involved in removing electrons from water; P680, reaction centre photosystem II complexis densely packed in the thylakoid chlorophyll of photosystem II; Pheo, pheophytin; QA, a bound plastoquinone; QB, plastoquinone that binds and unbinds from membrane, with average centre to centre distances of a few photosystem II; Tyr, a tyrosine residue in photosystem II (Yz); PQ, a pool of hundred angstroms. One square centimetre of a typical leaf mobile plastoquinone molecules. The antenna complexes are: LHC-II, contains about 30 trillion photosystem II complexes. peripheral light-harvesting complex of photosystem II; CP47 and CP43, Although photosystem II is found in prokaryotic chlorophyll–protein complexes of 47 and 43 kDa, respectively. cyanobacteria (e.g. Synechocystis spp.) and prochloro- phytes (e.g. Prochloron spp.), in eukaryotic green algae (e.g. Fucus spp.) and all higher plants (e.g. Arabidopsis (e.g. Chlamydomonas spp.), red algae (e.g. Porphyridium spp.), extensive research indicates that its structure and spp.), yellow-green algae (e.g. Vaucheria) and brown algae function are remarkably similar in these diverse organisms. 2 ENCYCLOPEDIA OF LIFE SCIENCES / & 2002 Macmillan Publishers Ltd, Nature Publishing Group / www.els.net Photosystem II Photosystem II is arranged as a central reaction centre