Unique organization of photosystem I–light-harvesting supercomplex revealed by cryo-EM from a red alga

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.

Abstract

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.