Integrated analyses of transcriptome, proteome and fatty acid profilings of the oleaginous microalga Auxenochlorella protothecoides UTEX 2341 reveal differential reprogramming of fatty acid metabolism in response to low and high temperatures

Temperature is one of the critical environmental factors that influence microalgal growth, lipid content and fatty acid (FA) composition. However, the molecular mechanism underlying regulations of FA metabolism under low and high temperature stress in oleaginous microalgae remains unclear. In this study, integrated analyses of transcriptome, proteome and fatty acid profilings were performed for the first time in Auxenochlorella protothecoides UTEX 2341. Under low and high temperature (LT and HT) stress, a total of 5565 and 4757 genes, and 1311 and 728 proteins were differentially expressed respectively. 65 actively expressed genes and 61 proteins involved in FA metabolism were identified. A strong positive correlation between the genes' transcript and protein levels existed in FA metabolism (r = 0.80, p-value < 0.01^⁎⁎, LT vs NT; r = 0.61, p-value < 0.01^⁎⁎, HT vs NT). Two models were proposed to reveal differential reprogramming of FA metabolism induced by low and high temperatures. Low temperature promoted chloroplast FA biosynthesis by enhancing the expression of the plastidial acetyl-CoA carboxylase (ACCase) and type-II fatty acid synthase. High temperature activated FA biosynthesis, including polyunsaturated and very-long-chain FAs in the cytosol and endoplasmic reticulum (ER) by increasing the expression of the cytosolic ACCase, type-I polyketide synthase and components of the ER-located elongase complex. The enhanced expression of the plastid-located pyruvate dehydrogenase complex (PDHC) and the suppressed FA β-oxidation also highly contributed to lipid accumulation. The biosynthesis of ω-3 fatty acid was closely related to microalgae's temperature adaptability. These results indicated that the reprogramming of FA metabolism was implicated in microalgae response to temperature stress. The above findings not only had important implications for the screening and genetic engineering of algae and plants to improve their lipid productions, but also provided novel insight into the adaptive mechanism to temperature stress.