Structure and energy transfer of a far-red-absorbing euglenophyte PSI-LhcE-LhcbM supercomplex

Euglenophyta originated from a secondary endosymbiosis between a phagotrophic euglenid and a green alga. Euglenophytes acquired photosynthesis-related genes from diverse algal lineages, representing a remarkable example of plastid evolution in the green lineage. Here, we solve the structure of the PSI-LhcE-LhcbM supercomplex from the euglenophyte Euglena gracilis. This supercomplex contains a simplified PSI core and an extensive antenna system, including 13 LhcEs and 2 LhcbMs. The LHCs are arranged as centrosymmetric dimers or monomers, resulting in a specific antenna organization. Notably, the LhcbMs are robustly integrated into the supercomplex through direct interactions with PsaB, PsaJ, and PsaF, without the need for phosphorylation. This phosphorylation-independent assembly mechanism highlights a specific adaptation in euglenophyte PSI-LhcE-LhcbM organization. We also identify specific structural features surrounding red-shifted chlorophyll a pairs in LHCs, which may account for the enhancement of far-red light absorption of PSI-LhcE-LhcbM. Computational simulations further reveal a distinctive pigment network, facilitating efficient energy transfer within the supercomplex. Our study not only provides insights into the mechanisms of light harvesting and energy transfer in euglenophyte PSI-LhcE-LhcbM but also broadens the framework of plastid evolution and complexity, with implications for modulation and bioengineering of photosynthetic complexes.