Trophic state alters the mechanism whereby energetic coupling between photosynthesis and respiration occurs in Euglena gracilis

The coupling between mitochondrial respiration and photosynthesis plays an important role in the energetic physiology of green plants and some secondary‐red photosynthetic eukaryotes (diatoms), allowing an efficient CO(2) assimilation and optimal growth. Using the flagellate Euglena gracilis, we first tested if photosynthesis–respiration coupling occurs in this species harbouring secondary green plastids (i.e. originated from an endosymbiosis between a green alga and a phagotrophic euglenozoan). Second, we tested how the trophic state (mixotrophy and photoautotrophy) of the cell alters the mechanisms involved in the photosynthesis–respiration coupling. Energetic coupling between photosynthesis and respiration was determined by testing the effect of respiratory inhibitors on photosynthesis, and measuring the simultaneous variation of photosynthesis and respiration rates as a function of temperature (i.e. thermal response curves). The mechanism involved in the photosynthesis–respiration coupling was assessed by combining proteomics, biophysical and cytological analyses. Our work shows that there is photosynthesis–respiration coupling and membrane contacts between mitochondria and chloroplasts in E. gracilis. However, whereas in mixotrophy adjustment of the chloroplast ATP/NADPH ratio drives the interaction, in photoautotrophy the coupling is conditioned by CO(2) limitation and photorespiration. This indicates that maintenance of photosynthesis–respiration coupling, through plastic metabolic responses, is key to E. gracilis functioning under changing environmental conditions.