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

Abstract

Abstract 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.