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.蓝细菌、藻类与植物通过产氧光合作用（oxygenic photosynthesis）固定二氧化碳并释放氧气。该过程依赖ATP与NADPH，二者由涉及多种多蛋白复合物与移动电子载体的光合光反应生成。这些复合物包含两类光系统（photosystem）：PSII与PSI，二者介导从水到NADP+分子的线性电子流（linear electron flow，LEF）。线性电子流可建立用于ATP合成的质子梯度，并介导NADP+的还原，该步骤需要PSI通过铁氧还蛋白（ferredoxin）提供电子。根据该经典模型，缺失PSI便无法进行线性电子流，因为PSI的缺失会阻断NADP+的还原过程。然而本研究证实，在蓝细菌集胞藻（Synechocystis PCC 6803）中，产氧光合作用可不依赖PSI而进行。通过适应性实验室进化实验，我们获得了PSI缺陷型菌株变体，该类菌株可在光合自养条件下维持生长。实现不依赖PSI的光合自养，需要两种及以上蛋白质发生共突变，其中包括翻译延伸因子G（translation elongation factor G，FusA）。当NDH-1复合物（NDH-1 complex）失活时，不依赖PSI的光合自养特性便会丧失，这表明NDH-1复合物可通过反向运作，将电子从质体醌（plastoquinone）传递至铁氧还蛋白，从而替代PSI的功能。本研究结果揭示了蓝细菌类囊体电子传递通路中此前未被发现的可塑性，这要求对现有的产氧光合作用模型进行修正。