Evolutionary origin and functional mechanism of Lhcx in the diatom photoprotection

Abstract

Diatoms are red-lineage algae that utilize the light-harvesting complex (LHC) subfamily Lhcx for photoprotection via non-photochemical quenching (NPQ); however, its evolutionary origin and molecular mechanism remain poorly understood. Through molecular phylogenetic analysis, we show that diatom Lhcxs and green algal Lhcsrs evolved from a common ancestor, with green plants subsequently acquiring them via horizontal gene transfer. To investigate the functional role of Lhcx1, we generated knockout mutants of Chaetoceros gracilis, a diatom with low Lhcx redundancy. The lhcx1 mutants nearly abolished NPQ, and time-resolved fluorescence measurements revealed that Lhcx1-mediated quenching occurs in energetically detached antenna complexes. Clear-native PAGE with Amphipol further indicated that CgLhcx1 interacts with the FCP L-dimer, functioning as a peripheral antenna for the C2S2M2 PSII-FCPII supercomplex. Notably, under high-light acclimation, lhcx1 mutants exhibited higher PSII effective quantum yields than wild type, attributable to reduced antenna size and enhanced carbon fixation capacity. The absence of NPQ accelerated high-light acclimation and was accompanied by increased xanthophyll accumulation, indicating that compensatory mechanisms can enhance overall photosynthetic efficiency. Together, these findings reveal the evolutionary origin of Lhcx/Lhcsr proteins and define the molecular basis of Lhcx1-mediated photoprotection in diatoms, providing fundamental insights into LHC-based photoprotection across photosynthetic lineages.