Cryptophyte algae are an important group of photosynthetic eukaryotes and originated evolutionarily from a secondary endosymbiosis with a red algal ancestor. Photosystem I (PSI) of cryptophyte algae binds alloxanthin-chlorophyll a/c-binding proteins (ACPs) equivalent to the light harvesting complexes (LHCs) of green algae and higher plants. Here, we report a high resolution (2.25 Å) structure of the PSI-ACPI supercomplex purified from the cryptophyte Chroomonas placoidea (C. placoidea) by cryo-electron microscopy. The PSI-ACPI supercomplex consists of a monomeric PSI core, 14 ACPI subunits and a Chl-binding subunit, CCPI-S. The 14 ACPI subunits are divided into two layers, with an inner layer including 11 ACPIs, and an outer layer consisting of 3 ACPIs. The CCPI-S mediates the connections and energy transfer between the outer and inner ACPI layers. Due to the current higher resolution, a unique PsaQ subunit bound at the lumenal side was identified in the PSI core. Two new pigment molecules Chl a856PsaA and Mon 627ACPI − 8 as well as 18 new lipids were identified, compared to the previously reported PSI-ACPI structure from the cryptophyte alga C. placoidea (Zhao et al. 2023). These lipids mediate the interactions of subunits and the assembly of PSI-ACPI. These results provide structural insights for the assembly of the PSI-ACPI complex and pathways of light-energy absorption and transfer in cryptophyte PSI-ACPI, as well as the possible adaptation mechanisms to fluctuating light conditions.