REVIEWS THE COMPLEX ARCHITECTURE OF OXYGENIC PHOTOSYNTHESIS Nathan Nelson and Adam Ben-Shem Abstract | Oxygenic photosynthesis is the principal producer of both oxygen and organic matter on earth. The primary step in this process — the conversion of sunlight into chemical energy — is driven by four, multisubunit, membrane-protein complexes that are known as photosystem I, photosystem II, cytochrome b6f and F-ATPase. Structural insights into these complexes are now providing a framework for the exploration not only of energy and electron transfer, but also of the evolutionary forces that shaped the photosynthetic apparatus. 8,9 PROTONMOTIVE FORCE Oxygenic photosynthesis — the conversion of sunlight After the invention of SDS–PAGE ,the biochemical (pmf). A special case of an into chemical energy by plants, green algae and composition of the four multisubunit protein com- electrochemical potential. It is cyanobacteria — underpins the survival of virtually all plexes began to be elucidated10–14.According to the par- the force that is created by the higher life forms. The production of oxygen and the tial reactions that they catalyse, PSII is defined as a accumulation of protons on one assimilation of carbon dioxide into organic matter water–plastoquinone oxidoreductase, the cytochrome-b f side of a cell membrane. This 6 concentration gradient is determines, to a large extent, the composition of our complex as a plastoquinone–plastocyanin oxidoreduc- generated using energy sources atmosphere and provides all life forms with essential tase, PSI as a plastocyanin–ferredoxin oxidoreductase such as redox potential or ATP. food and fuel. The study of the photosynthetic appara- and the F-ATPase as a pmf-driven ATP synthase15 (FIG. 1). Once established, the pmf can tus is a prime example of research that requires a com- PSI and PSII contain chlorophylls and other pigments be used to carry out work, for example, to synthesize ATP or to bined effort between numerous disciplines, which that harvest light and funnel its energy to a reaction pump compounds across the include quantum mechanics, biophysics, biochemistry, centre. Energy that has been captured by the reaction membrane. molecular and structural biology, as well as physiology centre induces the excitation of specialized reaction- and ecology. The time courses that are measured in centre chlorophylls (PRIMARY ELECTRON DONORS;a special photosynthetic reactions range from femtoseconds to chlorophyll pair in PSI), which initiates the transloca- days, which again highlights the complexity of this tion of an electron across the membrane through a process. chain of cofactors. Water, the electron donor for this Plant photosynthesis is accomplished by a series of process, is oxidized to O2 and 4 protons by PSII. The reactions that occur mainly, but not exclusively, in the electrons that have been extracted from water are shut- chloroplast (BOX 1).Initial biochemical studies showed tled through a quinone pool and the cytochrome-b6 f that the chloroplast thylakoid membrane is capable of complex to plastocyanin, a small, soluble, copper-con- light-dependent water oxidation, NADP reduction and taining protein16.Solar energy that has been absorbed ATP formation1.Biochemical and biophysical studies2–6 by PSI induces the translocation of an electron from Department of revealed that these reactions are catalysed by two sepa- plastocyanin at the inner face of the membrane (thy- Biochemistry, The George S. Wise rate photosystems (PSI and PSII) and an ATP synthase lakoid lumen) to ferredoxin on the opposite side Faculty of Life Sciences, (F-ATPase): the latter produces ATP at the expense of (stroma; FIG. 1). The reduced ferredoxin is subsequently Tel Aviv University, the PROTONMOTIVE FORCE (pmf) that is formed by the light used in numerous regulatory cycles and reactions, Tel Aviv 69978, Israel. reaction.The cytochrome-b f complex mediates elec- which include nitrate assimilation, fatty-acid desatura- Correspondence to N.N. 6 tron transport between PSII and PSI and converts the tion and NADPH production. The CHARGE SEPARATION e-mail: [email protected] redox energy into a high-energy intermediate (pmf) for in PSI and PSII, together with the electron transfer 7 doi:10.1038/nrm1525 ATP formation . through the cytochrome-b6 f complex, leads to the NATURE REVIEWS | MOLECULAR CELL BIOLOGY VOLUME 5 | DECEMBER 2004 | 1 © 2004 Nature Publishing Group REVIEWS unimportant. However, the lost QUANTA can inflict dam- Box 1 | The basic features of higher plant chloroplasts age on the photosynthetic complexes. In the less efficient Chloroplasts (see figure) are Chloroplast PSII, one of the subunits, D1,is turned over so fast that organelles that are bound by a its synthesis represents 50% of the total protein synthesis double membrane and are in chloroplasts, even though D1 actually represents only Stroma lamellae found in the cells of green ~0.1% of the total protein composition of chloro- plants and algae in which Thylakoid plasts21,22.Knowledge of the structures of, and pigment photosynthesis takes place. membranes distributions in, PSI and PSII should eventually help us They contain a third to explain the differences in their quantum yields and membrane system that is Stroma Grana Thylakoid lumen the consequences of these differences. In the following known as thylakoids, where all sections, we review the contribution of recent structural the pigments, electron- Inner membrane data to our understanding of the architecture and func- transport complexes and the Outer membrane tion of oxygenic photosynthesis. ATP synthase (F-ATPase) are located. The thylakoid membranes of higher plants consist of stacks of membranes that form the so-called granal regions.Adjacent grana are connected by non-stacked Photosystem II membranes called stroma lamellae. The fluid compartment that surrounds the thylakoids The PSII reaction centre is composed of two similar is known as the stroma, and the space inside the thylakoids is known as the lumen. ~40-kDa proteins (D1 and D2), which each consist of 5 transmembrane helices, and these proteins coordinate both the manganese cluster of PSII and all of the elec- formation of an ELECTROCHEMICAL-POTENTIAL gradient (the tron-transfer components23 (FIG. 2a).Flanking the reac- pmf), which powers ATP synthesis by the fourth protein tion centre are the intrinsic light-harvesting proteins PRIMARY ELECTRON DONORS 17 complex, F-ATPase .In the dark, CO2 reduction to car- CP43 and CP47,which each consist of 6 transmem- Reaction-centre chlorophyll pairs bohydrates is fuelled by ATP and NADPH18. brane helices and bind 14 and 16 chlorophyll-a mole- (P in PSI and P in PSII) that 700 680 24 are very different from antenna All of the four protein complexes that are necessary cules ,respectively. However, most of the chlorophylls chlorophylls.When they receive for the light-driven reactions of photosynthesis reside in that are associated with PSII are harboured in the light energy (from the antenna the chloroplast, in a membrane continuum of flattened extrinsic, peripheral light-harvesting complex II pigments), they generate a redox- vesicles called thylakoids (FIG. 1a;see also the BOX 1 (LHCII) antenna complexes. These are trimers of the active chemical species. Excited figure). In higher plants, thylakoids are differentiated light-harvesting proteins Lhcb1, Lhcb2 and Lhcb3, P680* donates an electron to another component of PSII, then into two distinct membrane domains — the cylindrical although each trimer can contain different stoichiome- eventually to the cytochrome-b6 f stacked structures known as grana and the intercon- tries of these proteins. The Lhcb proteins have a similar complex and to PSI.After necting single-membrane regions called stroma lamellae. structure, and harbour 12–14 chlorophyll-a and -b mol- donating the electron, P + — the 680 The four membrane complexes that drive the light reac- ecules and up to 4 CAROTENOIDS25,26.The number of strongest oxidant in biology — is tion are not evenly distributed throughout thylakoids: trimers that are associated with PSII varies with irradi- generated. P700* is the strongest + reductant in biology. P700 accepts PSI localizes to the stroma lamellae and is segregated ance level. Energy transfer from LHCII to CP43/CP47 an electron from plastocyanin. from PSII, which is almost exclusively found in the or D1/D2 is mediated by the minor light-harvesting grana; F-ATPase concentrates mainly in the stroma proteins Lhcb6 (CP24), Lhcb5 (CP26) and Lhcb4 CHARGE SEPARATION The process in which excited lamellae, whereas the cytochrome-b6 f complex prefer- (CP29), each of which is similar to an LHCII monomer. entially populates the grana and the grana margins19 The organization of the Lhcb proteins with the PSII P680* and P700* donate their electrons to their respective (FIG. 1a).The recent determination of the structures of reaction centre has been extensively studied using elec- acceptors to generate P + and 680 these complexes — or in the case of F-ATPase, of a close tron microscopy and several low-resolution models P +,respectively. 700 homologue from mitochondria — completes the have been described27,28. ELECTROCHEMICAL POTENTIAL description of the architecture of energy transduction PSII catalyses a unique process of water oxidation and Electrochemical potential is the in oxygenic photosynthesis that has been sought for provides almost all of the earth’s oxygen. Although some sum of the chemical potential the past 50 years (FIG. 1b).Here, we describe