Structural basis for far-red light harvesting in a euglenophyte photosystem II supercomplex

Abstract

Photosystem II (PSII) is in eukaryotic phototrophs is generally considered to operate within a more restricted spectral range than photosystem I (PSI), in which long-wavelength chlorophylls are a well-established feature of the peripheral antenna. Whether eukaryotic PSII can acquire comparable far-red-associated properties through lineage-specific antenna diversification has remained unclear. Here we present a 3.09 [A] cryo-electron microscopy structure of the C2S2M2L2 PSII supercomplex from Euglena gracilis, a euglenophyte species harbouring a secondary plastid and unusual light-harvesting system. We show that the euglenophyte-specific antenna protein LhcE9 occupies the position corresponding to canonical Lhcb5, but in a markedly different orientation that creates a distinct interface with the PSII core, particularly with CP43. Combined structural, spectroscopic, mutagenesis and proteomic analyses support LhcE9 as the stably bound PSII antenna subunit most closely associated with the far-red state in the supercomplex. Excitation-energy-transfer calculations further indicate two fast lineage-specific antenna-to-core routes mediated by LhcE9 and PsbX. Together, these findings reveal an unexpected mode of PSII antenna diversification and provide a structural framework for far-red-associated light harvesting in PSII.