Lipidomic and transcriptomic analyses of Chlamydomonas reinhardtii under heat stress unveil a direct route for the conversion of membrane lipids into storage lipids

Studying how photosynthetic cells modify membrane lipids in response to heat stress is important to understand how plants and microalgae adapt to daily fluctuations in temperature and to investigate new lipid pathways. Here, we investigate changes occurring in lipid molecular species and lipid metabolism genes during early response to heat stress in the model photosynthetic microorganism Chlamydomonas reinhardtii. Lipid molecular species analyses revealed that, after 60 min at 42 °C, a strong decrease in specific polyunsaturated membrane lipids was observed together with an increase in polyunsaturated triacylglycerols (TAGs) and diacylglycerols (DAGs). The fact that decrease in the major chloroplastic monogalactosyldiacylglycerol sn1‐18:3/sn2‐16:4 was mirrored by an accumulation of DAG sn1‐18:3/sn2‐16:4 and TAG sn1‐18:3/sn2‐16:4/sn3‐18:3 indicated that newly accumulated TAGs were formed via direct conversion of monogalactosyldiacylglycerols to DAGs then TAGs. Lipidomic analyses showed that the third fatty acid of a TAG likely originated from a phosphatidylethanolamine or a diacylglyceryl‐O‐4′‐(N,N,N,‐trimethyl)‐homoserine betaine lipid species. Candidate genes for this TAG synthesis pathway were provided through comparative transcriptomic analysis and included a phospholipase A2 homolog and the DAG acyltransferase DGTT1. This study gives insights into the molecular events underlying changes in membrane lipids during heat stress and reveals an alternative route for TAG synthesis. In the model photosynthetic organism Chlamydomonas reinhardtii, we show that the early response of plastidial membranes to heat stress involves selective reduction of polyunsaturated monogalactosylglycerol species by conversion to diacylglycerols and triacylglycerols. Candidate genes responsible for this conversion are identified by comparative transcriptomics of heat‐stressed to control cells.