Oxygenic photosynthesis without photosystem I in a cyanobacterium

Cyanobacteria, algae and plants use oxygenic photosynthesis to fix CO2 and release O2. This process depends on ATP and NADPH, which are produced by the photosynthetic light reactions involving several multi-protein complexes and mobile electron carriers. These complexes include the two photosystems, PSII and PSI, which support linear electron flow (LEF) from water to NADP+ molecules. LEF establishes a proton gradient for ATP formation and enables NADP+ reduction, a step which requires electron donation from PSI via ferredoxin. According to this model, LEF is impossible without PSI, as its absence would prevent NADP+ reduction. However, we present evidence here that oxygenic photosynthesis can occur independently of PSI in the cyanobacterium Synechocystis PCC 6803. Through adaptive laboratory evolution, we generated PSI-deficient strain variants that can sustain growth under photoautotrophic conditions. Achieving PSI-independent photoautotrophy required the co-mutation of two or more proteins, including the translation elongation factor G (FusA). PSI-independent photoautotrophy was lost when the NDH-1 complex was inactivated, suggesting that the NDH-1 complex can replace PSI when operating in reverse by transferring electrons from plastoquinone to ferredoxin. These findings reveal an unexpected plasticity in cyanobacterial thylakoid electron transport, necessitating a revision of existing models of oxygenic photosynthesis.