Photosystem I (PSI) is one of the two photosystems present in oxygenic photosynthetic organisms and functions to harvest and convert light energy into chemical energy in photosynthesis. In eukaryotic algae and higher plants, PSI consists of a core surrounded by variable species and numbers of light-harvesting complex (LHC)I proteins, forming a PSI-LHCI supercomplex. Here, we report cryo-EM structures of PSI-LHCR from the red alga in two forms, one with three Lhcr subunits attached to the side, similar to that of higher plants, and the other with two additional Lhcr subunits attached to the opposite side, indicating an ancient form of PSI-LHCI. Furthermore, the red algal PSI core showed features of both cyanobacterial and higher plant PSI, suggesting an intermediate type during evolution from prokaryotes to eukaryotes. The structure of PsaO, existing in eukaryotic organisms, was identified in the PSI core and binds three chlorophylls and may be important in harvesting energy and in mediating energy transfer from LHCII to the PSI core under state-2 conditions. Individual attaching sites of LHCRs with the core subunits were identified, and each Lhcr was found to contain 11 to 13 chlorophylls and 5 zeaxanthins, which are apparently different from those of LHCs in plant PSI-LHCI. Together, our results reveal unique energy transfer pathways different from those of higher plant PSI-LHCI, its adaptation to the changing environment, and the possible changes of PSI-LHCI during evolution from prokaryotes to eukaryotes.

Photosystem II (PSII) catalyzes light-induced water splitting, leading to the evolution of molecular oxygen indispensible for life on the earth. The crystal structure of PSII from cyanobacteria has been solved at an atomic level, but the structure of eukaryotic PSII has not been analyzed. Because eukaryotic PSII possesses additional subunits not found in cyanobacterial PSII, it is important to solve the structure of eukaryotic PSII to elucidate their detailed functions, as well as evolutionary relationships. Here we report the structure of PSII from a red alga Cyanidium caldarium at 2.76 Å resolution, which revealed the structure and interaction sites of PsbQ, a unique, fourth extrinsic protein required for stabilizing the oxygen-evolving complex in the lumenal surface of PSII. The PsbQ subunit was found to be located underneath CP43 in the vicinity of PsbV, and its structure is characterized by a bundle of four up-down helices arranged in a similar way to those of cyanobacterial and higher plant PsbQ, although helices I and II of PsbQ were kinked relative to its higher plant counterpart because of its interactions with CP43. Furthermore, two novel transmembrane helices were found in the red algal PSII that are not present in cyanobacterial PSII; one of these helices may correspond to PsbW found only in eukaryotic PSII. The present results represent the first crystal structure of PSII from eukaryotic oxygenic organisms, which were discussed in comparison with the structure of cyanobacterial PSII.Oxygenic photosynthesis provides us with food, oxygen, and fuel and is therefore vital to life on the earth. The first reaction occurring in oxygenic photosynthesis is the splitting of water into electrons, protons, and molecular oxygen, among which electrons and protons are utilized for the synthesis of NADPH and ATP, whereas oxygen is supplied to the atmosphere for maintaining aerobic life forms. The water splitting reaction is catalyzed by photosystem II (PSII), 5 an extremely large membrane-protein complex located in thylakoid membranes from prokaryotic cyanobacteria to higher plants. In the case of cyanobacteria, the crystal structure of PSII has been solved with its resolution gradually increased to an atomic level of 1.9 Å (1-6), which showed that PSII contains 17 transmembrane subunits and 3 peripheral, hydrophilic subunits with a total molecular mass of 700 kDa for a dimer.The first oxygenic photosynthetic organism is believed to be the ancestor of cyanobacteria some 2.7 billion years ago (7). Although the subunit compositions of PSII from cyanobacteria to higher plants we see today are rather conserved, some apparent differences exist in both the transmembrane and peripheral subunits among cyanobacteria, various algae, and higher plants (8). One of the remarkable differences is found in the composition and function of extrinsic proteins associated in the lumenal side and required for maintaining the optimal function of the water-splitting reaction. In cyanobacteria, three extrinsic proteins of PsbO (33 kDa), Ps...

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