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.

Centre Algatech Institute of Microbiology of the Czech Academy of Sciences Třeboň Czech Republic

Department of Biochemistry Faculty of Science Charles University Praha Czech Republic

Electron Microscopy Lab Imaging and Characterization Core Labs King Abdullah University of Science and Technology Thuwal Saudi Arabia

Faculty of Science University of South Bohemia České Budějovice Czech Republic

Institute of Microbiology of the Czech Academy of Sciences Prague Czech Republic

King Abdullah University of Science and Technology Biological and Environmental Science and Engineering Division Thuwal Saudi Arabia

School of Biosciences University of Sheffield Sheffield UK

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