期刊名称：Proceedings of the National Academy of Sciences
印刷版ISSN：0027-8424
电子版ISSN：1091-6490
出版年度：2022
卷号：119
期号：2
DOI：10.1073/pnas.2115261119
语种：English
出版社：The National Academy of Sciences of the United States of America
摘要：Significance
Photosynthetic organisms are responsible for the incorporation of inorganic carbon in the biosphere through a fundamental process known as carbon fixation. This reaction allows the reduction of inorganic carbon, mostly atmospheric CO
2, to organic compounds such as carbohydrates and amino acids. Despite the biological relevance of carbon fixation in nature, how photosynthetic cells sense carbon availability remains poorly understood. Using the model microalga
Chlamydomonas reinhardtii, we found that the photosynthetic assimilation of CO
2 regulates the activity of the target of rapamycin (TOR) kinase, a master regulator of cell growth and nutrient sensor widely conserved in all eukaryotes. Our study revealed that inorganic carbon fixation and photosynthesis regulate TOR activity, likely through the synthesis of central amino acids in carbon metabolism.
The target of rapamycin (TOR) kinase is a master regulator that integrates nutrient signals to promote cell growth in all eukaryotes. It is well established that amino acids and glucose are major regulators of TOR signaling in yeast and metazoan, but whether and how TOR responds to carbon availability in photosynthetic organisms is less understood. In this study, we showed that photosynthetic assimilation of CO
2 by the Calvin–Benson–Bassham (CBB) cycle regulates TOR activity in the model single-celled microalga
Chlamydomonas reinhardtii. Stimulation of CO
2 fixation boosted TOR activity, whereas inhibition of the CBB cycle and photosynthesis down-regulated TOR. We uncovered a tight link between TOR activity and the endogenous level of a set of amino acids including Ala, Glu, Gln, Leu, and Val through the modulation of CO
2 fixation and the use of amino acid synthesis inhibitors. Moreover, the finding that the
Chlamydomonas starch-deficient mutant
sta6 displayed disproportionate TOR activity and high levels of most amino acids, particularly Gln, further connected carbon assimilation and amino acids to TOR signaling. Thus, our results showed that CO
2 fixation regulates TOR signaling, likely through the synthesis of key amino acids.
