CO2-dependant promotion of photosynthesis drives metabolic photoacclimation in Chlamydomonas reinhardtii.

Light and inorganic carbon (C i ) 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 C i availability in algae remains elusive. Here, we characterised bioenergetics and profiled primary metabolites of photoautotrophic Chlamydomonas reinhardtii cultures grown under constant low/sub-saturating (LL) or high/saturating (HL) light with 2 % (CO 2 ) or ambient 0.04 % (Amb) CO 2 . HL-Amb cells suffered photoinhibition and limitation of photosystem I electron flow at the donor side, but not 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-CO 2 cells upregulated the cytochrome b 6 f 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. CO 2 -enhanced photosynthesis promoted respiration and primary metabolite accumulation, driving faster growth while promoting nitrogen (N) metabolism. Hence, C i -dependant photoacclimation influenced the interplay between the TCA cycle and N assimilation, as supported by proteomic data. Overall, abundant C i supported growth by promoting electron flow for C i assimilation, which supplied C skeletons for N assimilation, while mitigating photorespiration and photoinhibition.