Architecture of symbiotic dinoflagellate photosystem I–light-harvesting supercomplex in Symbiodinium

Abstract

Symbiodinium are the photosynthetic endosymbionts for corals and play a vital role in supplying their coral hosts with photosynthetic products, forming the nutritional foundation for high-yield coral reef ecosystems. Here, we determine the cryo-electron microscopy structure of Symbiodinium photosystem I (PSI) supercomplex with a PSI core composed of 13 subunits including 2 previously unidentified subunits, PsaT and PsaU, as well as 13 peridinin-Chl a/c-binding light-harvesting antenna proteins (AcpPCIs). The PSI–AcpPCI supercomplex exhibits distinctive structural features compared to their red lineage counterparts, including extended termini of PsaD/E/I/J/L/M/R and AcpPCI-1/3/5/7/8/11 subunits, conformational changes in the surface loops of PsaA and PsaB subunits, facilitating the association between the PSI core and peripheral antennae. Structural analysis and computational calculation of excitation energy transfer rates unravel specific pigment networks in Symbiodinium PSI–AcpPCI for efficient excitation energy transfer. Overall, this study provides a structural basis for deciphering the mechanisms governing light harvesting and energy transfer in Symbiodinium PSI–AcpPCI supercomplexes adapted to their symbiotic ecosystem, as well as insights into the evolutionary diversity of PSI–LHCI among various photosynthetic organisms.

Structure of cryptophyte photosystem II–light-harvesting antennae supercomplex

“…Using our structural data, we computationally simulated the excitation energy transfer (EET) between pigments within PSII–ACPII following the process as reported previously 40 . We assumed energy transfer in the limit of Förster theory, which is a generally accepted method for estimating the rate of energy transfer between two pigments that possess small interactions 41 .…”

“…Pigments extracted from 30 μL concentrated sample by 120 μL pre-cooled 100% acetone overnight at 4 °C were injected into C18 reversed-phase column (Waters, Ireland). The pigment extraction and the elution procedure were performed as described previously 40 , 59 . The eluates were detected by photodiode array detector at 445 nm.…”

“…High-throughput sequencing of C. placoidea transcriptome was performed by BioMarker (BMK) following the previously reported procedure 40 . Total RNA was extracted from cells.…”

“…The sequences of the C. placoidea PSII core identified in the transcriptome were used for correcting the amino acid residues of each chain. The sequences of PsbW and subunit Psb-γ were searched from the transcriptome using the estimated sequences based on the cryo-EM map as previously described 40 . The potential sequences of ACPIIs were searched from the transcriptome using the sequences of ACPI-1/2/3/12/13/14.…”

“…Excitation energy transfer within PSII–ACPII was studied in the limit of the Förster theory as previously described 40 , 41 . The energy transfer rates between Chls, T values in ps −1 , were calculated using the following equation: …”