Dark respiration modulates photosynthetic carbon yield in cyanobacteria

Cyanobacteria contribute to roughly a quarter of global net carbon fixation. During diel light/dark growth, dark respiration significantly lowers the overall photosynthetic carbon yield in cyanobacteria and other phototrophs. Currently, it is unclear how respiratory pathways participate in allocating carbon resources at night to optimize dark survival and support daytime photosynthesis. Here we show in the cyanobacterium Synechococcus elongatus PCC 7942 that phosphoketolase is orchestrated in an integrative respiratory network in the dark to best allocate carbon resource for amino acid synthesis and prepare for photosynthesis reinitiation upon photoinduction. We further show that the respiratory Entner-Doudoroff (ED) pathway in S. elongatus is incomplete, with its key enzyme 2-keto-3-deoxy-6-phosphogluconate (KDPG) aldolase serving to modulate daytime photosynthesis through an alternative oxaloacetate decarboxylation activity. This activity allows for the bypassing of the tricarboxylic acid (TCA) cycle when ATP/NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Optimizing these metabolic processes offers new opportunities to enhance photosynthetic carbon yield in cyanobacteria and other photosynthetic organisms under diel light/dark cycles.