The architecture and energy transfer pathways of PSI-LHCI-LHCII in the phototrophic flagellate Euglena gracilis.

Abstract

Photosystem I (PSI) harvests light through light-harvesting complexes (LHCs) to drive electron transfer. Euglena gracilis, a secondary endosymbiotic green alga, yet the architecture of its PSI-LHCs supercomplex has remained unresolved. Here, we report a 2.06 Å cryo-electron microscopy structure of the E. gracilis PSI-LHCI-LHCII supercomplex, revealing a minimal PSI core associated with ten antennas arranged in two layers on the PsaM-facing side. Each inner and outer LHC forms a face-to-face pair, while four LHCI heterodimers, stabilized by conserved Loop_23 motifs, assemble into two tetramers bridged by a central LHCI-LHCII pair. Notably, a ~ 40-residue insertion in PsaD was observed, anchoring LHC-3 and stabilizing LHC belts. Moreover, Euglena-specific chlorophylls and a distinctive arrangement of red chlorophylls establish a distinct pigment network, channeling excitation-energy into the core. These findings uncover a lineage-specific strategy for light-harvesting, highlighting how secondary plastids remodel PSI-LHCs architecture to support photosynthesis.