Choreography of Transcriptomes and Lipidomes of Nannochloropsis Reveals the Mechanisms of Oil Synthesis in Microalgae[W][OPEN]

To reveal the molecular mechanisms underlying lipid accumulation in microalgae, transcriptomic and lipidomic dynamics of Nannochloropsis oceanica under nitrogen-replete and nitrogen-depleted conditions were simultaneously tracked. The temporal and spatial regulation model established in this study provides a basis for the rational genetic engineering of enhanced oil production. To reveal the molecular mechanisms of oleaginousness in microalgae, transcriptomic and lipidomic dynamics of the oleaginous microalga Nannochloropsis oceanica IMET1 under nitrogen-replete (N+) and N-depleted (N-) conditions were simultaneously tracked. At the transcript level, enhanced triacylglycerol (TAG) synthesis under N- conditions primarily involved upregulation of seven putative diacylglycerol acyltransferase (DGAT) genes and downregulation of six other DGAT genes, with a simultaneous elevation of the other Kennedy pathway genes. Under N- conditions, despite downregulation of most de novo fatty acid synthesis genes, the pathways that shunt carbon precursors from protein and carbohydrate metabolic pathways into glycerolipid synthesis were stimulated at the transcript level. In particular, the genes involved in supplying carbon precursors and energy for de novo fatty acid synthesis, including those encoding components of the pyruvate dehydrogenase complex (PDHC), glycolysis, and PDHC bypass, and suites of specific transporters, were substantially upregulated under N- conditions, resulting in increased overall TAG production. Moreover, genes involved in the citric acid cycle and β-oxidation in mitochondria were greatly enhanced to utilize the carbon skeletons derived from membrane lipids and proteins to produce additional TAG or its precursors. This temporal and spatial regulation model of oil accumulation in microalgae provides a basis for improving our understanding of TAG synthesis in microalgae and will also enable more rational genetic engineering of TAG production.

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