Glycogen metabolism jump-starts photosynthesis through the oxidative pentose phosphate pathway (OPPP) in cyanobacteria

Abstract

Cyanobacteria experience drastic changes in their carbon metabolism under daily light-dark cycles. In the light, the Calvin-Benson cycle fixes CO2 and divert excess carbon into glycogen storage. At night, glycogen is degraded to support cellular respiration. Dark-light transition represents a universal environmental stress for cyanobacteria and other photosynthetic lifeforms. Recent studies in the field revealed the essential genetic background necessary for the fitness of cyanobacteria during diurnal growth. However, the metabolic engagement behind the dark-light transition is not well understood. In this study, we discovered that glycogen metabolism can jump-start photosynthesis in the cyanobacterium Synechococcus elongatus PCC 7942 when photosynthesis reactions start upon light. Compared to the wild type, the glycogen mutant (ΔglgC) showed much lower photosystem II efficiency and slower photosystem I-mediated cyclic electron flow rate when photosynthesis starts. Proteomics analyses indicated that glycogen is degraded through the oxidative pentose phosphate pathway (OPPP) during dark-light transition. We confirmed that the OPPP is essential for the initiation of photosynthesis, and further showed that glycogen degradation through the OPPP is likely to contribute to the activation of key Calvin-Benson cycle enzymes by modulating NADPH levels during the transition period. This ingenious strategy helps jump-start photosynthesis in cyanobacteria following dark respiration, and stabilize the Calvin-Benson cycle under fluctuating environmental conditions. It has evolutionary advantages for the survival of photosynthetic organisms using the Calvin-Benson cycle for carbon fixation.