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The complex architecture of oxygenic photosynthesis

Nature Reviews Molecular Cell Biology volume 5, pages 971–982 (2004)Cite this article

A Correction to this article was published on 01 October 2005

Key Points

  • The process of oxygenic photosynthesis, in which solar energy is converted into chemical energy, underpins life on earth and is the principal producer of both oxygen and organic matter on earth.

  • Oxygenic photosynthesis is driven by four large membrane-protein complexes that reside in the thylakoid membranes of cyanobacteria, algae and plants. The structure of three of these assemblies (photosystem I, photosystem II and the cytochrome-b6f complex) were recently solved by X-ray crystallography, and the structure of the fourth (ATP synthase or F-ATPase) can be deduced from its mitochondrial relative, the structure of which is largely known.

  • In photosystem II, a cluster of four manganese ions, plus a calcium ion and a chloride ion, is responsible for water oxidation. A recent structure sheds light on the arrangement of this cluster and provides important insights into the mechanism of light-dependant oxygen evolution.

  • Structures of the cytochrome-b6f complex — which mediates electron transfer between photosystem II and photosystem I — have, surprisingly, revealed the position of unexpected cofactors that might have an important role in cyclic photophosphorylation.

  • A recently solved structure of plant photosystem I provides the first example of a supercomplex, which is composed of a reaction centre similar to that of cyanobacteria and a light-harvesting complex that is unique to the chloroplasts of eukaryotes.

  • Together, the structures of these complexes form a unique body of information that has helped us to understand the architecture of oxygenic photosynthesis, which is one of the most intricate and fundamental processes of life.

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.

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Figure 1: The structures of the four large membrane-protein complexes in thylakoid membranes that drive oxygenic photosynthesis.
Figure 2: The structure of photosystem II and the cofactors that are involved in light-induced water oxidation and plastoquinone reduction.
Figure 3: The structure of the cytochrome-b6f complex from Chlamydomonas reinhardtii and the cofactors that are involved in its mechanism of action.
Figure 4: A view from the stroma on plant photosystem I.
Figure 5: A model for the interaction of plant photosystem I with its electron donors/acceptors and the pathways for light-induced electron transport.
Figure 6: A composit model for the structure of the chloroplast F-ATPase.

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Acknowledgements

We would like to thank W. Frasch for the use of his structural model of F-ATPase (figure 6). A.B.-S. is a recipient of a Charles Clore Foundation Ph.D. student scholarship. The work of N.N. is supported by the Israel Science Foundation.

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  1. Department of Biochemistry, The George S. Wise Faculty of Life Sciences, Tel Aviv University, Tel Aviv, 69978, Israel

    Nathan Nelson & Adam Ben-Shem

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  1. Nathan Nelson
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Correspondence to Nathan Nelson.

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DATABASES

Protein Data Bank

1A70

1AG6

1JBO

1Q90

1QZV

1S5L

Swiss-Prot

human cytochrome b

human cytochrome c

TAIR

CP24

CP26

CP29

CP43

CP47

cytochrome b6

cytochrome f

D1

D2

PetG

PsaA

PsaC

PsaI

PsaJ

Rieske iron–sulphur protein

subunit IV

Glossary

PROTONMOTIVE FORCE

(pmf). A special case of an electrochemical potential. It is the force that is created by the accumulation of protons on one side of a cell membrane. This concentration gradient is generated using energy sources such as redox potential or ATP. Once established, the pmf can be used to carry out work, for example, to synthesize ATP or to pump compounds across the membrane.

PRIMARY ELECTRON DONORS

Reaction-centre chlorophyll pairs (P700 in PSI and P680 in PSII) that are very different from antenna chlorophylls. When they receive light energy (from the antenna pigments), they generate a redox-active chemical species. Excited P680* donates an electron to another component of PSII, then eventually to the cytochrome-b6f complex and to PSI. After donating the electron, P680+ — the strongest oxidant in biology — is generated. P700* is the strongest reductant in biology. P700+ accepts an electron from plastocyanin.

CHARGE SEPARATION

The process in which excited P680* and P700* donate their electrons to their respective acceptors to generate P680+ and P700+, respectively.

ELECTROCHEMICAL POTENTIAL

Electrochemical potential is the sum of the chemical potential (concentration difference across the membrane) and the electrical potential (charge-concentration difference across the membrane).

QUANTUM YIELD

In a particular system, the number of defined electronic or chemical events that occur per photon absorbed.

QUANTA

Specific packets of electromagnetic energy (also known as photons). They have no mass, but they do have a momentum. Photosynthetic organisms capture the momentum of a photon and translate it into biological energy.

CAROTENOID

Any of a class of yellow to red pigments, which include carotenes and xanthophylls.

REDOX POTENTIAL

Redox potential is a measure (in volts) of the affinity of a substance for electrons. This value for each substance is compared to that for hydrogen, which is set arbitrarily at zero. Substances that are more strongly oxidizing than hydrogen have positive redox potentials (oxidizing agents), whereas substances that are more reducing than hydrogen have negative redox potentials (reducing agents).

KOK–JOLIOT FIVE S-STATES

The oxidation of water to oxygen occurs at the oxygen-evolving complex/manganese cluster in photosystem II. This cluster cycles through five states (S0–S4) during the oxidation process, and this cycle was discovered by Bessel Kok and Pierre Joliot about four decades ago.

RIESKE IRON–SULPHUR PROTEIN

A subunit of the cytochrome-bc1 and -b6f complexes that contains an iron–sulphur cluster.

Q CYCLE

The mechanism by which the cytochrome-bc1 and -b6f complexes achieve their energy transduction to generate a protonmotive force.

CHLOROPHYLL TRIPLET

A chlorophyll with unpaired valence electrons. It can interact with molecular oxygen to form singlet oxygen. This, in turn, is a highly reactive molecule that might destruct nearby proteins or other biologically important molecules.

STATE TRANSITION

A short-term response to light conditions, in which plants can differentially distribute light energy between photosystem I and photosystem II. It is thought to occur through the relocation of light-harvesting complex II between the two photosystems.

CALVIN CYCLE

The Calvin cycle is a metabolic pathway that occurs in the stroma of chloroplasts, in which carbon enters in the form of CO2 and leaves in the form of sugar. The cycle uses ATP as an energy source and NADPH as a reducing agent.

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Nelson, N., Ben-Shem, A. The complex architecture of oxygenic photosynthesis. Nat Rev Mol Cell Biol 5, 971–982 (2004). https://doi.org/10.1038/nrm1525

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