Back to the Seabed: The Unique Photosystem I Architecture of the Seagrass Posidonia oceanica

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Abstract

Seagrasses are marine angiosperms re-adapted to underwater life, forming productive ecosystems and long-term carbon sinks. Posidonia oceanica thrives up to 50 m depth, where light is scarce and spectrally shifted; yet, the molecular basis of its photosynthetic adaptation remains unclear. We showed that P. oceanica is genetically adapted to perform highly efficient photon use under dim light by enhancing photosystems antenna size and reducing exciton trapping time. We solved the structures of P. oceanica PSI supercomplexes by cryo-electron microscopy, revealing an expanded antenna system composed of PSI-LHCI, a trimeric phospho-LHCII, and an additional LHCI heterodimer. Low-energy chlorophyll spectral forms associated to LHCI, which modulate antenna-to-reaction center excitation transfer, are lost. Ultrafast spectroscopy revealed that this loss results in faster exciton trapping, thus compensating for antenna expansion and loss of quantum efficiency under dim light. Key residues responsible for the loss of low-energy forms were identified; replacing them with land-plant orthologs restored red-shifted emission, providing strategies to enhance light-use efficiency in crops.

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