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Abstract Cryptophytes are ancestral photosynthetic organisms evolved from red algae through secondary endosymbiosis. They have developed alloxanthin-chlorophyll a/c2-binding proteins (ACPs) as light-harvesting complexes (LHCs). The distinctive properties of cryptophytes contribute to efficient oxygenic photosynthesis and underscore the evolutionary relationships of red-lineage plastids. Here we present the cryo-electron microscopy structure of the Photosystem II (PSII)–ACPII supercomplex from the cryptophyte Chroomonas placoidea. The structure includes a PSII dimer and twelve ACPII monomers forming four linear trimers. These trimers structurally resemble red algae LHCs and cryptophyte ACPI trimers that associate with Photosystem I (PSI), suggesting their close evolutionary links. We also determine a Chl a-binding subunit, Psb-γ, essential for stabilizing PSII–ACPII association. Furthermore, computational calculation provides insights into the excitation energy transfer pathways. Our study lays a solid structural foundation for understanding the light-energy capture and transfer in cryptophyte PSII–ACPII, evolutionary variations in PSII–LHCII, and the origin of red-lineage LHCIIs.

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. [ABSTRACT FROM AUTHOR]