In situ structural basis for the LHCSR3-mediated photoprotection of photosystem II

Energy-dependent quenching (qE) represents a critical mechanism for photosynthetic organisms to mitigate photodamage caused by excessive light. In green algae, LHCSR3 protein plays a central role in qE, activated by thylakoid lumen acidification and associated with photosystem II (PSII) to dissipate excess energy. Despite extensive efforts, the assembly and energy dissipation mechanisms of PSII-LHCSR3 have remained unknown. Here, we present the in situ structures of the PSII supercomplex embedded in the native thylakoid membranes of Chlamydomonas reinhardtii in both quenched (LHCSR3-bound) and unquenched (LHCSR3-free) states at near-atomic resolutions. Our results demonstrate that in high-light-acclimated cells, LHCSR3 binds to PSII peripheral antenna CP26 and associates with an extra LHCII trimer (eLHCII). Structural comparison of LHCSR3 with other light-harvesting complexes reveals possible protonation-induced conformational changes in LHCSR3 and rearrangements of its two pigment clusters, which potentially serve as quenching sites to dissipate excess energy transferred from CP26 and eLHCII. Our findings provide a direct visualization of how photoprotection is spatially organized in vivo and have implications for engineering natural and artificial photosynthetic systems with more dynamic photoprotection.