Plastid-encoded Ycf10 maintains chloroplast proton homeostasis essential for photosynthesis in Chlamydomonas reinhardtii

Chloroplasts in plants and algae are vital for photosynthesis. During photosynthesis an appropriate proton balance needs to be maintained across the thylakoid membranes within chloroplasts for regulating key processes such as synthesis of ATP and NADPH, inorganic carbon transport, and non-photochemical quenching. While the chloroplast gene ycf10 has been associated with inorganic carbon uptake in Chlamydomonas reinhardtii, its function in regulating proton homeostasis and coordinating photosynthetic acclimation processes remains unclear. In this study, mutants with inactivated ycf10 were generated in Chlamydomonas reinhardtii. These mutants showed impaired growth, reduced photosynthetic activity, and inability to efficiently induce non-photochemical quenching. Further analysis revealed changes in the proton motive force (pmf) and proton accumulation in the cytoplasm under high light stress, indicating a potential role for Ycf10 in maintaining proton homeostasis. Notably, growth impairment under acidic conditions was alleviated by increasing pH, highlighting the importance of proton balance for photosynthesis and growth. Additionally, loss of Ycf10 function reduced inorganic carbon affinity under acidic pH and compromised CO2 fixation under high light stress. Ycf10 dysfunction also led to excess ROS accumulation, triggering autophagy. These findings indicate that Ycf10 is crucial for chloroplast proton homeostasis, optimizing photosynthesis and growth.