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 that is evolutionary linked to parasitic apicomplexans, exhibits Photosystem I with unusual features. These include the splitting of the central PsaA subunit and the binding of superoxide dismutases as regular subunits. The organization of such a unique Photosystem I was enigmatic. Here, we present the cryo-EM structure of Chromera velia Photosystem I at 1.84 Å resolution. Our work reveals a superoxide dismutase heterodimer bound to the stromal side of the core, stabilized by extensions of canonical subunits, a novel protein PsaV, and a reduced light-harvesting apparatus. We elucidate how the complex evolved to accommodate the superoxide dismutase, assemble the split PsaA, and integrate antenna proteins in a non-canonical orientation. Based on our data and prior physiological data, we propose that this specialized Photosystem I functions likely as an Mehler 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.
© 2025. The Author(s).