In photosynthesis, the plant photosystem II uses the energy in sunlight to oxidize water. The high-resolution structure of this crucial supercomplex has now been obtained using cryo-electron microscopy. See Article p.69
Photosystem II is the enzyme complex that produces the oxygen we breathe. It is at the heart of the photosynthesis process, and uses the energy of the Sun to extract from water the electrons and protons that are needed to produce food and fuel. On page 69 of this issue, Wei et al.1 report the structure of spinach photosystem II — a 1.1-megadalton dimeric complex in which each monomer is composed of 25 proteins and 133 pigment molecules. This structure provides a plethora of information to aid our understanding of the molecular mechanisms by which light is converted into chemical energy.
Photosystem II (PSII) is a membrane-embedded modular assembly of pigment–protein complexes and is composed of two main parts, the core and the outer antenna. The core contains the reaction centre in which energy is used to drive photochemistry. It has an evolutionarily highly conserved protein composition in all the organisms that perform oxygen-generating photosynthesis2.
Wei and colleagues' structure shows that both the protein and the pigment organization of the plant PSII core in the membrane region are almost identical to those of the core of the previously reported3 structure of cyanobacterial PSII; this indicates that the complex was optimized long ago and has not changed since. Only the peripheral membrane proteins that surround the water-splitting catalyst in the core are organized differently in plants and cyanobacteria. This observation is intriguing, because these peripheral proteins are needed for oxidizing water4, and their organizational differences from their cyanobacterial counterparts might inform how nature has optimized this essential reaction.
In contrast to the core, the outer antenna differs greatly between photosynthetic organisms. Its role is to increase the core's capacity to harvest light, overcoming the fact that light is a dilute form of energy (one molecule of the pigment chlorophyll absorbs only a few photons per second even on a bright, sunny day). The outer antenna is shaped by the host organism's adaptation to its ecological niche, where light quantity and quality vary, and thus it is tailor-made5. In vascular plants (including spinach), the outer antenna is composed of light-harvesting complexes (LHCs). These are pigment–protein complexes that absorb light and transfer part of the corresponding energy to the reaction centre.
In the present structure, each monomer of the PSII supercomplex is composed of a core, one LHC trimer (called LHCII; ref. 6) and one monomer of each of two minor LHCs, CP29 and CP26 . Wei and colleagues' work offers the first structures of the plant PSII core, CP26 and the complete CP29. It also shows the position of the core subunit PsbW and the molecular details of the connection between the antenna and the core (Fig. 1). Notably, the long amino-terminal region of CP29 extends all the way over the CP47 subunit of the core to interact with the D1 protein of the reaction centre. This organization provides a structural basis for the observation7 that, in plants, LHCs are required for the connectivity in the core.
A substantial problem in obtaining structural information about plant PSII has been its instability, which is a direct consequence of its functional behaviour. Not only must PSII adjust its antenna size in response to natural lighting conditions, but it must also repair its reaction centre; splitting water using sunlight is a risky business that can lead to the generation of reactive oxygen species, which damage the system. To repair the damage, PSII undergoes regular 'pit stops', during which it is disassembled and reassembled after substitution of the damaged part8. Cryo-electron microscopy was therefore crucial in solving this structure, because it allowed Wei et al. to select the intact particles from the ensemble and reach an amazing 3.2-ångström resolution.
Although modularity is required to allow repair, a good connection between the subunits is equally important for efficient energy transfer from the antenna to the core. The absorption of a photon promotes chlorophyll to an excited state, but this state is unstable and the chlorophyll relaxes to its initial (ground) state within a few nanoseconds. Once back to the ground state, the energy is lost. Consequently, time is limited for using the energy, which must then be rapidly transferred to the reaction centre.
Earlier work showed7 that in the plant PSII supercomplex, it takes 140 picoseconds (1 ps is 10−12 s) from the absorption of a photon by a chlorophyll molecule to the charge separation in the reaction centre, such that more than 90% of the photons absorbed produce an electron. How fast this energy is transferred from the antenna to the reaction centre depends on the distance between the pigments, their relative orientation and their energy. These factors are all dictated by the proteins, which act as smart matrices that organize the pigments.
The LHCs contain two types of chlorophyll (a and b) that are chemically similar but energetically different. Chlorophyll a absorbs lower-energy photons than chlorophyll b. Because energy preferentially migrates downstream, chlorophyll b rapidly transfers it to chlorophyll a; the energy is then transferred to the reaction centre mainly by chlorophyll a.
Although detailed computational modelling based on the new structure is needed for a quantitative understanding of the excitation-energy transfer, visual inspection of how chlorophylls are organized in the supercomplex already provides qualitative indications. Intriguingly, the interface between the LHCs is occupied by chlorophyll b molecules located relatively far from each other, suggesting that there is little (if any) transfer of energy between the LHCs present in this supercomplex. Instead, all LHCs seem to transfer their collected energy directly to the core.
This organization may seem at odds with the required efficiency, because more energy-transfer pathways normally result in higher efficiency9. In cells, however, PSII is in contact with other LHCs, the number of which varies under different conditions and which are not present in the isolated supercomplex10. The presence of chlorophyll a at the periphery of the supercomplex can help to transfer energy from such additional LHCs to the core.
Clearly, Wei et al. have provided us with a wonderful structure. The ball is now in the court of spectroscopists and theoreticians to use this structure to obtain a detailed understanding of the functionality of the system. Footnote 1
Wei, X. et al. Nature 534, 69–74 (2016).
Hohmann-Marriott, M. F. & Blankenship, R. E. Annu. Rev. Plant Biol. 62, 515–548 (2011).
Umena, Y., Kawakami, K., Shen, J.-R. & Kamiya, N. Nature 473, 55–60 (2011).
Ifuku, K. Biosci. Biotechnol. Biochem. 79, 1223–1231 (2015).
Croce, R. & van Amerongen, H. Nature Chem. Biol. 10, 492–501 (2014).
Liu, Z. et al. Nature 428, 287–292 (2004).
Caffarri, S., Broess, K., Croce, R. & van Amerongen, H. Biophys. J. 100, 2094–2103 (2011).
Järvi, S., Suorsa, M. & Aro, E.-M. Biochim. Biophys. Acta Bioenerget. 1847, 900–909 (2015).
Chmeliov, J., Trinkunas, G., van Amerongen, H. & Valkunas, L. J. Am. Chem. Soc. 136, 8963–8972 (2014).
Dekker, J. P. & Boekema, E. J. Biochim. Biophys. Acta 1706, 12–39 (2005).