Structural insights into the assembly and energy transfer of haptophyte photosystem I–light-harvesting supercomplex

Haptophyta represents a major taxonomic group, with plastids derived from the primary plastids of red algae. Here, we elucidated the cryoelectron microscopy structure of the photosystem I-light-harvesting complex I (PSI-LHCI) supercomplex from the haptophyte Isochrysis galbana. The PSI core comprises 12 subunits, which have evolved differently from red algae and cryptophytes by losing the PsaO subunit while incorporating the PsaK subunit, which is absent in diatoms and dinoflagellates. The PSI core is encircled by 22 fucoxanthin-chlorophyll a/c-binding light-harvesting antenna proteins (iFCPIs) that form a trilayered antenna arrangement. Moreover, a pigment-binding subunit, LiFP, which has not been identified in any other previously characterized PSI-LHCI supercomplexes, was determined in I. galbana PSI-iFCPI, presumably facilitating the interactions and energy transfer between peripheral iFCPIs and the PSI core. Calculation of excitation energy transfer rates by computational simulations revealed that the intricate pigment network formed within PSI-iFCPI ensures efficient transfer of excitation energy. Overall, our study provides a solid structural foundation for understanding the light-harvesting and energy transfer mechanisms in haptophyte PSI-iFCPI and provides insights into the evolution and structural variations of red-lineage PSI-LHCIs.