The molecular structure of Photosystem I from Chromera velia: A Mehler machine at 1.84 A resolution

Photosystem I is a key component of the solar energy conversion machinery in oxygenic photosynthesis, and its core, where photochemistry occurs, is highly conserved. However, the coral-associated alga Chromera velia, which occupies a unique evolutionary position between photosynthetic algae and parasitic apicomplexans, exhibits Photosystem I with highly unusual features. These include the splitting of the central PsaA subunit and the binding of superoxide dismutases as novel regular subunits. The organization of such a unique Photosystem I has remained enigmatic. Here, we present the cryo-EM structure of Chromera. velia Photosystem I at 1.84 Å resolution. Our analysis reveals a superoxide dismutase heterodimer bound to the stromal side of the core, stabilized by extensions of canonical subunits, two newly identified proteins (Psa34 and Psa35), and a reduced light-harvesting apparatus featuring a uniquely bound xanthophyll. We elucidate how the complex evolved to accommodate the superoxide dismutase, assemble the split PsaA subunit, and integrate antenna proteins in a non-canonical orientation. Based on our structural insights and prior physiological data, we propose that this specialized Photosystem I functions as an oxygen-photo-reduction machine, redirecting electrons from Photosystem II back to water. This mechanism enables Chromera. velia to manage redox imbalance and reduce photorespiration through localized oxygen consumption. The high-resolution model presented here provides a foundation for future biotechnological applications aimed at optimizing photosynthetic design in diverse taxa.