Marine phytoplankton are responsible for a half of global primary production, playing fundamental roles in supporting food webs as well as driving vertical carbon export to the deep ocean. In past few decades, extensive efforts have been made to reveal how cyanobacteria and eukaryotic algae fix inorganic carbon through diverse photosynthetic machineries. In contrast, their respiratory metabolisms, which can lead to significant biomass carbon loss (equivalent to that caused by heterotrophic respiration in surface oceans), have attracted insufficient attention. In this context, our recent studies using cyanobacteria as a model reveal important physiological roles of several historically overlooked or mischaracterized enzymes in the respiratory pathways, and how they compose integrative networks to support robust photoautotrophic growth in naturally fluctuating light conditions (Xie et al, The Plant Cell, 2025; Xie et al, Plant Physiology, in revision). For example, we show that phosphoketolase integrates into a respiratory network in the dark to best allocate carbon resources for amino acid biosynthesis and to prepare for photosynthesis reinitiation upon photoinduction. Moreover, we show that the respiratory Entner–Doudoroff pathway is incomplete in phototrophs, with its key enzyme KDPG aldolase exhibiting alternative oxaloacetate decarboxylation activity that modulates daytime photosynthesis in cyanobacteria; this activity allows for the bypassing of the tricarboxylic acid cycle when ATP and NADPH consumption for biosynthesis is excessive and imbalanced relative to their production by the light reactions, thereby preventing relative NADPH accumulation and ensuring optimal photosynthetic carbon yield. Our unpublished work further reveals photoprotective roles of carbon metabolisms associated with glycogen phosphorylase and phosphoenolpyruvate synthase in acclimation to high light stresses through differential mechanisms. Proteomics and metabolomics data suggest a broader range of flexible and integrative metabolic responses of cyanobacteria to light dynamics in their natural environments. These results provide novel and crucial insights on how phytoplankton regulate their metabolism to ensure fitness under diel cycles or during sinking/upwelling. As the basis of marine food webs and the biological carbon pump, phytoplankton impact not only the euphotic but also the deep ocean microbiomes and ecosystems. Our field observations on marine fungus-like protists suggest their patchy co-blooms with phytoplankton in the surface ocean, potentially leading to fast-sinking aggregates and significant biomass contribution to the deep ocean microbiomes. Our current and future work is integrating oceanographical observations with physiological studies to discover and examine metabolic plasticity in diverse phytoplankton as well as their interactions with important heterotrophic taxa, revealing the cascade effects on marine carbon cycles and sequestration.
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