Photosystem I-independent oxygenic photosynthesis in cyanobacteria

Oxygenic photosynthesis in cyanobacteria, algae, and plants fixes carbon dioxide and releases oxygen. This process depends on ATP and NADPH generated by light-driven reactions involving multi-protein complexes and mobile electron carriers. Central to these reactions are Photosystem II (PSII) and Photosystem I (PSI), which enable linear electron flow (LEF) from water to NADP ⁺ molecules ¹ . LEF both drives proton gradient formation for ATP synthesis and supports NADP ⁺ reduction via ferredoxin-mediated electron transfer from PSI ^2–4 . According to prevailing models, LEF cannot occur without PSI, as its absence would block NADP⁺ reduction. Here we show that oxygenic photosynthesis can take place independently of PSI in the cyanobacterium Synechocystis PCC 6803. Through adaptive laboratory evolution, we obtained PSI-deficient lineages capable of photoautotrophic growth, inorganic carbon fixation, and light-dependent oxygen evolution. PSI-independent photoautotrophy emerged following co-mutations in at least two proteins, including the translation elongation factor G (FusA), and was abolished when the NDH-1 complex was disrupted. These results suggest that NDH-1 can substitute for PSI by operating in reverse to transfer electrons from plastoquinone to ferredoxin. Our findings reveal an unanticipated plasticity in the thylakoid electron transport network of cyanobacteria and compel a revision of existing models of oxygenic photosynthesis.