In a study published in Science Advances, a team co-led by Assoc. Prof. WANG Yumei from the Institute of Physics of the Chinese Academy of Sciences and TIAN Lirong from Hebei Normal University resolved the high-resolution structure of the Euglena gracilis photosystem I-light-harvesting complex (PSI-LHCE) supercomplex, offering insights into the structural diversity and evolutionary adaptation of oxygenic photosynthetic machinery in a secondary endosymbiotic organism.

Euglena gracilis is a flagellate alga that arose through a secondary endosymbiotic event between a phagotrophic euglenid and green algae ancestors, making it an interesting example in the evolution of plastids in the green lineage. It has a mixed nutritional strategy and a mosaic genome that includes genes from different algal sources, but until now there has been limited atomic-level information on how its photosynthetic machinery, especially PSI, is structured and functions.

In this study, the researchers resolved the high-resolution structure of the Euglena gracilis PSI-LHCE supercomplex at 2.23 Å using cryo-electron microscopy (cryo-EM). The cryo-EM data were acquired at the Beijing National Laboratory for Condensed Matter Physics. The structure showed that the PSI-LHCE supercomplex is much more diverse in composition than typical green lineage PSI complexes.

Instead of having identical copies of antenna proteins, the researchers found that the complex contains 16 peripheral antenna subunits that come from 12 different Lhca proteins and four distinct Lhcbm proteins. Such a high level of diversity in the antenna system had not been seen in other known photosynthetic systems and suggested that Euglena gracilis recruits a variety of light harvesting proteins to better capture sunlight in changing aquatic environments.

In terms of pigment composition, the Euglena gracilis PSI core and antenna system showed a clear "red-green mosaic" feature. All antenna proteins were bounded with carotenoid diadinoxanthin (Ddx), which is typical of red lineage algae. Four Ddx molecules were identified in positions within the PSI core where green lineage species normally have β-carotene. This finding provides evidence at the atomic level that Euglena gracilis combines pigment features from different algal lineages.

In addition, the researchers found that the PSI-LHCE complex has a "small core, large antenna" organization. Structural analysis showed that the LHCE subunits form tight internal connections by packing together through their transmembrane helices, rather than being held together mainly by interactions with the PSI core. This finding suggests that interactions between antenna units themselves play a major role in stabilizing the overall complex.

This study provides a robust structural foundation for elucidating the mechanisms of light harvesting and energy transfer as well as insights into the evolutionary changes of green-lineage PSI-LHCI.