Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO₂ conditions. When light energy exceeds CO₂ fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO₂ Concentrating Mechanism (CCM). How light and CO₂ signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO₂ concentrations and that depletion of CO₂ drives these responses, even in total darkness. High CO₂ levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3/CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO₂ and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO₂ levels.

In nature, photosynthetic organisms are exposed to different light spectra and intensities depending on the time of day and atmospheric and environmental conditions. When photosynthetic cells absorb excess light, they induce nonphotochemical quenching to avoid photodamage and trigger expression of “photoprotective” genes. In this work, we used the green alga Chlamydomonas reinhardtii to assess the impact of light intensity, light quality, photosynthetic electron transport, and carbon dioxide on induction of the photoprotective genes ( LHCSR1 , LHCSR3 , and PSBS ) during dark-to-light transitions. Induction (mRNA accumulation) occurred at very low light intensity and was independently modulated by blue and ultraviolet B radiation through specific photoreceptors; only LHCSR3 was strongly controlled by carbon dioxide levels through a putative enhancer function of CIA5, a transcription factor that controls genes of the carbon concentrating mechanism. We propose a model that integrates inputs of independent signaling pathways and how they may help the cells anticipate diel conditions and survive in a dynamic light environment.

Availability of light and CO₂, substrates of microalgae photosynthesis, is frequently far from optimal. Microalgae activate photoprotection under strong light, to prevent oxidative damage, and the CO₂ Concentrating Mechanism (CCM) under low CO₂, to raise intracellular CO₂ levels. The two processes are interconnected; yet, the underlying transcriptional regulators remain largely unknown. Employing a large transcriptomic data compendium of Chlamydomonas reinhardtii’s responses to different light and carbon supply, we reconstruct a consensus genome-scale gene regulatory network from complementary inference approaches and use it to elucidate transcriptional regulators of photoprotection. We show that the CCM regulator LCR1 also controls photoprotection, and that QER7, a Squamosa Binding Protein, suppresses photoprotection- and CCM-gene expression under the control of the blue light photoreceptor Phototropin. By demonstrating the existence of regulatory hubs that channel light- and CO₂-mediated signals into a common response, our study provides an accessible resource to dissect gene expression regulation in this microalga.

In photosynthetic organisms, light acts as an environmental signal to control their development and physiology, as well as energy source to drive the conversion of CO₂ into carbohydrates used for growth or storage. The main storage carbohydrate in green algae is starch, which accumulates during the day and is broken down at night to meet cellular energy demands. The signaling role of light quality in the regulation of starch accumulation remains unexplored. Here, we identify PHOTOTROPIN-MEDIATED SIGNALING KINASE 1 (PMSK1) as a key regulator of starch metabolism in Chlamydomonas reinhardtii. In its phosphorylated form (PMSK1-P), it activates GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE (GAP1), promoting starch biosynthesis. We show that blue light, perceived by PHOTOTROPIN, induces PMSK1 dephosphorylation that in turn represses GAP1 mRNA levels and reduces starch accumulation. These findings reveal a previously uncharacterized blue light-mediated signaling pathway that advances our understanding of photoreceptor-controlled carbon metabolism in microalgae.

In nature, photosynthetic organisms are exposed to different light spectra and intensities depending on the time of day and atmospheric and environmental conditions. When photosynthetic cells absorb excess light, they induce non-photochemical quenching to avoid photo-damage and trigger expression of ‘photoprotective’ genes. In this work, we used the green alga Chlamydomonas reinhardtii to assess the impact of light intensity, light quality, wavelength, photosynthetic electron transport and CO ₂ on induction of the ‘photoprotective’ genes ( LHCSR1 , LHCSR3 and PSBS ) during dark-to-light transitions. Induction (mRNA accumulation) occurred at very low light intensity, was independently modulated by blue and UV-B radiation through specific photoreceptors, and only LHCSR3 was strongly controlled by CO ₂ levels through a putative enhancer function of CIA5, a transcription factor that controls genes of the carbon concentrating mechanism. We propose a model that integrates inputs of independent signaling pathways and how they may help the cells anticipate diel conditions and survive in a dynamic light environment.

Photosynthetic algae have evolved mechanisms to cope with suboptimal light and CO ₂ conditions. When light energy exceeds CO ₂ fixation capacity, Chlamydomonas reinhardtii activates photoprotection, mediated by LHCSR1/3 and PSBS, and the CO ₂ Concentrating Mechanism (CCM). How light and CO ₂ signals converge to regulate these processes remains unclear. Here, we show that excess light activates photoprotection- and CCM-related genes by altering intracellular CO ₂ concentrations and that depletion of CO ₂ drives these responses, even in total darkness. High CO ₂ levels, derived from respiration or impaired photosynthetic fixation, repress LHCSR3 /CCM genes while stabilizing the LHCSR1 protein. Finally, we show that the CCM regulator CIA5 also regulates photoprotection, controlling LHCSR3 and PSBS transcript accumulation while inhibiting LHCSR1 protein accumulation. This work has allowed us to dissect the effect of CO ₂ and light on CCM and photoprotection, demonstrating that light often indirectly affects these processes by impacting intracellular CO ₂ levels.