CO2-Dependent Promotion of Photosynthesis Drives Metabolic Photoacclimation in Chlamydomonas reinhardtii.

Light and inorganic carbon (Ci) drive photosynthesis, which fuels cellular maintenance, energy storage, and growth in photosynthetic organisms. Despite its pivotal role, how primary metabolism adjusts to contrasting light and Ci availability in algae remains elusive. Here, we characterized bioenergetics and profiled primary metabolites of photoautotrophic Chlamydomonas reinhardtii cultures grown under constant low/sub-saturating (LL) or high/saturating (HL) light with 2% (CO2) or ambient 0.04% (Amb) CO2. HL-Amb cells suffered photoinhibition and limitation of photosystem I electron flow at the donor side, but not the acceptor side, indicating use of alternative electron pathways to fuel ATP synthesis. Further, more glycolate was excreted under HL-Amb, indicative of photorespiration. In contrast, HL-CO2 cells upregulated the cytochrome b6f complex, ascorbate metabolism, and PTOX2 for maintaining plastid redox homeostasis. Enhanced glycerol excretion under HL enabled dissipation of excess reducing equivalents to adjust the cellular energy balance. CO2-enhanced photosynthesis promoted respiration and primary metabolite accumulation, driving faster growth while promoting nitrogen (N) metabolism. Hence, Ci-dependent photoacclimation influenced the interplay between the TCA cycle and N assimilation, as supported by proteomic data. Overall, abundant Ci supported growth by promoting electron flow for Ci assimilation, which supplied C skeletons for N assimilation while mitigating photorespiration and photoinhibition.