Photosystem I enters into the spotlight: Plants rely on large complexes of proteins, chlorophyll, and other cofactors to turn light into chemical energy. Qin et al. present the crystal structures of photosystem I (PSI) and the light-harvesting complex I (LHCI) supercomplex from pea plants (see the Perspective by Croce). The well-resolved structure of the outer antenna complexes and their interaction with the PSI core provide a structural basis for calculating excitation energy transfer efficiency. Moreover, the organization and orientation of chlorophyll and carotenoid cofactors within and between PSI and LHCI hint at energy transfer and photoprotection mechanisms. Science , this issue p. 989 ; see also p. 970

All the hues, even the blues: Photosynthetic organisms must balance maximizing productive light absorption and protecting themselves from too much light, which causes damage. Both tasks require pigments—chlorophylls and carotenoids—which absorb light energy and either transfer it to photosystems or disperse it as heat. Wang et al. determined the structure of a fucoxanthin chlorophyll a/c–binding protein (FCP) from a diatom. The structure reveals the arrangement of the specialized photosynthetic pigments in this light-harvesting protein. Fucoxanthin and chlorophyll c absorb the blue-green light that penetrates to deeper water and is not absorbed well by chlorophylls a or b. FCPs are related to the light-harvesting complexes of plants but have more binding sites for carotenoids and fewer for chlorophylls, which may help transfer and disperse light energy. Science , this issue p. eaav0365

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 Cyanidioschyzon merolae 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 a 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 a 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. Significance Photosystem I (PSI) is one of the most efficient nanophotochemical machines in nature. To adapt to various environments, photosynthetic organisms developed different PSI structure during evolution from prokaryotic cyanobacteria to higher plants. Red algae are one of the most primitive eukaryotic algae, and their photosynthetic apparatus represents a transitional state between cyanobacteria and eukaryotes. We determined two forms of the PSI-LHCR structure from a red alga by cryo-EM. Our results revealed unique features and energy transfer pathways in the red algal PSI supercomplex with LHCI (light-harvesting complex I), as well as its remarkable differences with those of cyanobacterial PSI and higher plant PSI-LHCI. These results provide important information for delineating the function and evolution of PSI from prokaryotic to eukaryotic photosynthetic organisms.

Plants harvest light energy utilized for photosynthesis by light-harvesting complex I and II (LHCI and LHCII) surrounding photosystem I and II (PSI and PSII), respectively. During the evolution of green plants, moss is at an evolutionarily intermediate position from aquatic photosynthetic organisms to land plants, being the first photosynthetic organisms that landed. Here, we report the structure of the PSI–LHCI supercomplex from the moss Physcomitrella patens (Pp) at 3.23 Å resolution solved by cryo-electron microscopy. Our structure revealed that four Lhca subunits are associated with the PSI core in an order of Lhca1–Lhca5–Lhca2–Lhca3. This number is much decreased from 8 to 10, the number of subunits in most green algal PSI–LHCI, but the same as those of land plants. Although Pp PSI–LHCI has a similar structure as PSI–LHCI of land plants, it has Lhca5, instead of Lhca4, in the second position of Lhca, and several differences were found in the arrangement of chlorophylls among green algal, moss, and land plant PSI–LHCI. One chlorophyll, PsaF–Chl 305, which is found in the moss PSI–LHCI, is located at the gap region between the two middle Lhca subunits and the PSI core, and therefore may make the excitation energy transfer from LHCI to the core more efficient than that of land plants. On the other hand, energy-transfer paths at the two side Lhca subunits are relatively conserved. These results provide a structural basis for unravelling the mechanisms of light-energy harvesting and transfer in the moss PSI–LHCI, as well as important clues on the changes of PSI–LHCI after landing.