In the model organism Chlamydomonas reinhardtii, photosynthesis and aerobic respiration occur in chloroplasts and mitochondria, respectively, while anaerobic fermentation can occur independently in the cytoplasm, mitochondria and chloroplasts. How these three basic energy metabolism processes occur in harmony and order within the same cell is a scientific question that deserves deeper consideration. Currently, there is a relative paucity of research surrounding the interactions among the three, and the mechanism of functional coupling is not yet clear.
Previous studies have shown that photosynthetic organisms gradually accumulate protons under dark treatment, leading to acidification of the chloroplast-like vesicle lumen and thus inhibition of photosynthesis, which may be related to chloroplast respiration or ATP hydrolysis. Based on the previous studies on the acidification of the cystoid lumen, Tian Lijin's research group at the Institute of Botany, Chinese Academy of Sciences, hypothesized that the weak acid produced during the fermentation process might have inhibited photosynthesis. In order to test this hypothesis, the study integrated biological, physical and chemical methods, and found that the addition of weak acids under dark conditions could cause acidification of the cyst lumen in the chloroplast respiration mutants ptox2, nda2 and ATP hydrolysis mutant FUD50, which excluded the assertion that acidification of the cyst lumen in the dark was caused by chloroplast respiration and ATP hydrolysis, respectively. Meanwhile, it was found that the degree of acidification in the cyst lumen was positively correlated with the total accumulation of anaerobically metabolized weak acids, whereas no acidification was detected in experiments using the green alga NIES-2499, which is a non-producer of weak acids during fermentation metabolism, under the same treatment conditions. This suggests that the weak acid metabolite produced by fermentation is the causative agent for acidification of the cystoid lumen. The study also demonstrated that this feedback regulation mechanism of metabolites exists in different species of photosynthetic organisms. Further, based on the semi-permeability of the membrane to small molecules, the study proposed the "ion trap" model, i.e., the weak acid molecules produced by exogenous addition or anaerobic fermentation can cross the lipid bilayer and finally enter the cystoid lumen, but the ionized ions are not able to freely cross the membrane, and the cystoid lumen has a lower pH buffering capacity, which leads to the accumulation of protons in the lumen and acidification. and thus acidification occurs.
This study elucidates a new mechanism by which anaerobic fermentation affects photosynthesis and respiration in photosynthetic organisms, which is of great significance for exploring the chemical coupling between photosynthesis, aerobic respiration and anaerobic respiration, and for investigating the basic physiological processes of photosynthetic organisms, as well as optimizing the growth and carbon sequestration capacity of plants.
The related research results were published online in Nature Communications. Researchers from the Free University of Amsterdam, the Netherlands, the University of Liège, Belgium, and CNRS, France, participated in the study. The research was supported by the National Key Research and Development Program of China, the National Natural Science Foundation of China and the Strategic Pilot Project of the Chinese Academy of Sciences.
Metabolic pathway of anaerobic fermentation in Chlamydomonas reinhardtii and a working model of the "ion trap"
