Architecture and energy transfer of coccolithophore photosystem I with a huge light-harvesting antenna system

Coccolithophores play important roles in global biogeochemical cycles and climate change and are characterized by their cell surfaces covered with calcium carbonate coccoliths. Their capacity to thrive in dynamic marine ecosystems is underpinned by efficient photosynthetic adaptation. Here, we elucidated the structure of a photosystem I-light-harvesting complex I (PSI-LHCI) supercomplex from coccolithophore Emiliania huxleyi by cryo-electron microscopy, ultrafast spectroscopy, and computational simulations. The PSI core is encircled by 35 LHCIs that are organized in six layers with repetitive, fiber-like arrangements, forming a giant PSI-LHCI supercomplex. Increased levels of chlorophylls c and carotenoids in LHCIs enhance the absorption of blue/green light. Time-resolved spectral analysis and computational simulations both revealed that the large number of pigments forms an extensive pigment network, ensuring efficient energy transfer from peripheral LHCIs to the PSI core. Our study provides insights into the assembly and energy transfer of coccolithophore PSI-LHCI and delineates the evolutionary variation of red-lineage PSI-LHCIs.