Energetic robustness to large scale structural dynamics in a photosynthetic supercomplex

Dvir Harris ¹ Hila Toporik ^2,3 Yuval Mazor ^2,3 Gabriela Schlau-Cohen ¹

¹Faculty of Chemistry, Massachusetts Institute of Technology, USA
²School of Molecular Sciences, Arizona State University, USA
³Biodesign Institute, School of Molecular Sciences, Arizona State University, USA

Photosynthetic organisms transport and convert solar energy with near-unity quantum efficiency using large supercomplexes found in flexible cellular membranes. Individual proteins position pigments within tight tolerances considered critical for fast and efficient energy transfer. The variability in the protein organization, and how efficiency is maintained despite this variability, had been unresolved.

Here, we report the structural heterogeneity in the cryo-EM data of the 2-MDa cyanobacterial Photosystem I-Iron Starvation-Induced Protein A (PSI-IsiA) supercomplex, revealing large-scale variances in the IsiA positions relative to PSI. Corresponding single-molecule measurements found efficient IsiA-to-PSI energy transfer across all conformations, along with signatures of transiently decoupled IsiA. Structure based calculations showed that rapid IsiA-to-PSI energy transfer is maintained over most conformations and increases by up to 3-fold in rare conformations via IsiA-specific chlorophylls.

We postulate that antennae design mitigates structural fluctuations, providing a mechanism for energy transfer robustness in the flexible membrane.