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

Abstract

Higher plant Photosystem I (PSI) can capture low-energy photons and convert them into chemical energy through special far-red absorbing chlorophylls, the red-forms. Across higher-plant evolution, red-form spectral range has shifted to match differences in far-red availability across various habitats, despite broad conservation of the antenna system and canonical red-form architecture. Here, we report the 1.9 A cryo-EM structure of a large and blue shifted PSI light-harvesting complex I and II supercomplex (L-PSI-LHCI-LHCII) from the Mediterranean seagrass Posidonia oceanica, a marine angiosperm adapted to blue-enriched underwater light depleted in far-red wavelengths. Although the PSI core remains conserved, the antenna system was selectively remodeled through incorporation of an additional Lhca1-Lhca4 heterodimer at a previously undescribed binding site, together with pigment remodeling in the LHCI and the LHCII that enhanced blue-cyan light harvesting. Comparative structural analyses identified recurrent amino-acid sites within the far-red domains that influence red-forms geometry and whose residue composition diverges strongly among blue-shifted and red-shifted plant species. These findings establish a common structural basis underlying the spectral diversification of PSI toward contrasting light environments, accounting for both seagrass adaptation to the seawater light regime and the broad range of far-red absorption in higher plants.