Contribution of LHCE proteins to far-red light absorption and photosynthetic dynamics in Euglena gracilis

The evolution of oxygenic photosynthesis, converting solar energy into chemical energy, plays a pivotal role in directly or indirectly sustaining most terrestrial life forms. Euglena gracilis, an excavate unicellular eukaryote, has adopted secondarily photosynthesis following a kleptoplasty event between a green alga and an ancient phagotrophic euglenozoan species. Revisiting previous phylogenomic analyses of the light-harvesting complex (LHC) protein family has unveiled the absence of canonical LHCA proteins in Euglena gracilis, while introducing a new family of LHC proteins (referred to as LHCE). We investigated whether LHCE proteins might modulate the light- harvesting capacity in E. gracilis. Under far-red/near-infrared light (720-940 nm) or very low white light, the absorption spectrum of E. gracilis revealed an additional peak at 695 nm. Notably, under these conditions, the antenna sizes at 720-730 nm of photosystem II (PS II) were observed to be larger. This far-red absorption capacity is usually attributed to the presence of "red" or "low-energy" chlorophylls. Through the separation of photosynthetic machinery components in their native form via gel electrophoresis, we indeed identified a 250-kD complex containing only chlorophyll a and diadinoxanthin, which exhibited red-shifted absorption and fluorescence spectra, correlating with in vivo spectral changes. This complex likely comprises 5 LHCE antenna proteins unique to Euglena gracilis. Moreover, this LHCE antenna complex demonstrates rapid dissociation or reassociation with Photosystem II within a few minutes in response to far-red-enriched light, akin to the classical State Transition process. In conclusion, our study demonstrates that Euglena gracilis adjusts the antenna size of PSII by expressing a LHCE protein complex involved in chromatic adaptation and photon capture dynamics.