Photosystem II (PSII) in the thylakoid membranes of plants, algae, and cyanobacteria catalyzes light-induced oxidation of water by which light energy is converted to chemical energy and molecular oxygen is produced. In higher plants and most eukaryotic algae, the PSII core is surrounded by variable numbers of light-harvesting antenna complex II (LHCII), forming a PSII–LHCII supercomplex. In order to harvest energy efficiently at low–light-intensity conditions under water, a complete PSII–LHCII supercomplex (C ₂ S ₂ M ₂ N ₂ ) of the green alga Chlamydomonas reinhardtii (Cr) contains more antenna subunits and pigments than the dominant PSII–LHCII supercomplex (C ₂ S ₂ M ₂ ) of plants. The detailed structure and energy transfer pathway of the Cr-PSII–LHCII remain unknown. Here we report a cryoelectron microscopy structure of a complete, C ₂ S ₂ M ₂ N ₂ -type PSII–LHCII supercomplex from C. reinhardtii at 3.37-Å resolution. The results show that the Cr-C ₂ S ₂ M ₂ N ₂ supercomplex is organized as a dimer, with 3 LHCII trimers, 1 CP26, and 1 CP29 peripheral antenna subunits surrounding each PSII core. The N-LHCII trimer partially occupies the position of CP24, which is present in the higher-plant PSII–LHCII but absent in the green alga. The M trimer is rotated relative to the corresponding M trimer in plant PSII–LHCII. In addition, some unique features were found in the green algal PSII core. The arrangement of a huge number of pigments allowed us to deduce possible energy transfer pathways from the peripheral antennae to the PSII core.

Photosystem II (PSII) uses solar energy to oxidize water and delivers electrons for life on Earth. The photochemical reaction center of PSII is known to possess two stationary states. In the open state (PSII_O), the absorption of a single photon triggers electron-transfer steps, which convert PSII into the charge-separated closed state (PSII_C). Here, by using steady-state and time-resolved spectroscopic techniques on Spinacia oleracea and Thermosynechococcus vulcanus preparations, we show that additional illumination gradually transforms PSII_C into a light-adapted charge-separated state (PSII_L). The PSII_C-to-PSII_L transition, observed at all temperatures between 80 and 308 K, is responsible for a large part of the variable chlorophyll-a fluorescence (F_v) and is associated with subtle, dark-reversible reorganizations in the core complexes, protein conformational changes at noncryogenic temperatures, and marked variations in the rates of photochemical and photophysical reactions. The build-up of PSII_L requires a series of light-induced events generating rapidly recombining primary radical pairs, spaced by sufficient waiting times between these events—pointing to the roles of local electric-field transients and dielectric relaxation processes. We show that the maximum fluorescence level, F_m, is associated with PSII_L rather than with PSII_C, and thus the F_v/F_m parameter cannot be equated with the quantum efficiency of PSII photochemistry. Our findings resolve the controversies and explain the peculiar features of chlorophyll-a fluorescence kinetics, a tool to monitor the functional activity and the structural-functional plasticity of PSII in different wild-types and mutant organisms and under stress conditions.

Photosystem I (PSI) and II (PSII) balance their light energy distribution absorbed by their light-harvesting complexes (LHCs) through state transition to maintain the maximum photosynthetic performance and to avoid photodamage. In state 2, a part of LHCII moves to PSI, forming a PSI-LHCI-LHCII supercomplex. The green alga Chlamydomonas reinhardtii exhibits state transition to a far larger extent than higher plants. Here we report the cryo-electron microscopy structure of a PSI-LHCI-LHCII supercomplex in state 2 from C. reinhardtii at 3.42 Å resolution. The result reveals that the PSI-LHCI-LHCII of C. reinhardtii binds two LHCII trimers in addition to ten LHCI subunits. The PSI core subunits PsaO and PsaH, which were missed or not well-resolved in previous Cr-PSI-LHCI structures, are observed. The present results reveal the organization and assembly of PSI core subunits, LHCI and LHCII, pigment arrangement, and possible pathways of energy transfer from peripheral antennae to the PSI core.

Green to the core: Light from the Sun powers most life on today's Earth in some way. The core of the photosynthetic apparatus where charge separation occurs, the reaction center (RC), is thought to have originated a single time and diverged, yielding new kinds of complexes adapted to different tasks and environments. Chen et al. now present an important missing puzzle piece in our understanding of the evolution of RCs: a cryo–electron microscopy structure of the homodimeric type I RC from a green sulfur bacterium bound to a light-harvesting protein. The observed cofactor and pigment arrangement explain biochemical features of this RC and will aid in our understanding of how a single ancestral RC gave rise to the range of structures and functions seen in RCs today. Science , this issue p. eabb6350

Significance: Photosystem II (PSII) is a light-driven water:plastoquinone oxidoreductase in oxygenic photosynthetic organisms. Several inactive PSII intermediates are involved in the biogenesis of the multisubunit PSII complexes as well as in their repair after unavoidable oxidative damage targeted to PSII under light. Psb27 is one of the assembly factors associated with inactive PSII intermediate and plays important roles in the biogenesis/repair of PSII. Here, we report the structure of a dimeric Psb27-PSII from a thermophilic cyanobacterium Thermosynechococcus vulcanus by cryo-electron microscopy. Our results reveal the location and binding properties of Psb27 in the intermediate PSII and show the structural differences between the intermediate and native PSII. These results provide important clues for the roles of Psb27 in the biogenesis/repair of PSII.