The Posidonia oceanica Large PSI–LHCII supercomplex reveals the molecular basis of PSI spectral diversification in higher plants

ABSTRACT Photosystem I (PSI) in higher plants retains a largely conserved architecture, consisting of a PSI core associated with four canonical light-harvesting proteins (antenna) that host far-red-absorbing chlorophylls, the red forms. Across higher-plant evolution, PSI spectral properties diversified extensively, adapting light harvesting to its availability across habitats, particularly in the far-red range. This diversification occurred despite the conservation of the antenna system and the red-forms, prompting the investigation of its structural basis. Here, we report the 1.9 Å cryo-EM structure of a large PSI light-harvesting complex I and II supercomplex (L-PSI-LHCI-LHCII) from the Mediterranean seagrass Posidonia oceanica , characterized by blue-shifted absorption and strongly attenuated red forms. The antenna of this complex comprises a canonically bound LHCII trimer and six Lhca proteins: the two canonical Lhca1-Lhca4/Lhca2-Lhca3 heterodimers, plus an additional Lhca1–Lhca4 dimer attached via a new binding site but which engages amino-acid residues largely conserved in both seagrasses and land angiosperms. The sub-2 Å map further revealed blue-light adaptation through pigment substitutions in the LHCs, while structure comparison with land angiosperms identified recurrent amino-acid site around the red forms whose residue composition (i) subtly affects the red forms geometry and (ii) diverges strongly among blue-shifted and red-shifted plant species. These findings reveal the structural basis underlying PSI spectral diversification, accounting for both seagrass adaptation to the seawater light regime and the broad range of far-red absorption in higher plants.