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

Abstract

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 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, C_i-dependent 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.