Miranda-Astudillo, H.; Arshad, R.; Vega de Luna, F.; Aguilar-Gonzalez, Z.; Foret, H.; Feller, T.; Gervasi, A.; Nawrocki, W.; Counson, C.; Morsomme, P.; Degand, H.; Baurain, D.; Kouril, R.; Cardol, P.

Photosynthetic organisms have evolved diverse strategies to adapt to fluctuating light conditions, balancing efficient light capture with photoprotection. In green algae and land plants, this involves specialized light-harvesting complexes (LHCs), non-photochemical quenching, and state transitions driven by dynamic remodeling of antenna proteins associated with Photosystems (PS) I and II. Euglena gracilis, a flagellate with a secondary green plastid, represents a distantly related lineage whose light-harvesting regulation remains poorly understood. Although spectral shifts under different light regimes have been observed, their molecular basis was unknown. Here, through integrated phylogenomic, proteomic, structural, and spectroscopic analyses, we identify a novel chlorophyll a far-red-absorbing antenna complex in E. gracilis, composed of a species-specific Lhce protein family. This antenna forms a pentameric complex under low light and transiently associates with PSII during far-red light exposure. It is structurally and functionally distinct from canonical LHCII trimers and absent in Viridiplantae. Additionally, PSI in E. gracilis is surrounded by an expanded Lhce/LhcbM belt around a minimal core. These findings reveal a unique mechanism for regulating PS antenna size in E. gracilis, distinct from known models in plants and green algae, and highlight an alternative evolutionary strategy for light acclimation in organisms with secondary plastids.