Abstract
Microalgae are a promising feedstock for biofuel production. Microalgal metabolic pathways are heavily influenced by environmental factors. For instance, lipid metabolism can be induced by nitrogen-limiting conditions. However, the underlying mechanisms of lipid biosynthesis are unclear. In this study, we analyzed the global metabolic profiles of three genetically closely related Chlorella strains (C1, C2, and C3) with significant differences in lipid productivity to identify the contributions of key metabolic pathways to lipid metabolism. We found that nitrogen obtained from amino acid catabolism was assimilated via the glutamate–glutamine pathway and then stored as amino acids and intermediate molecules (particularly proline, alanine, arginine, succinate, and gamma-aminobutyrate) via the corresponding metabolic pathways, which led to carbon–nitrogen disequilibrium. Excess carbon obtained from photosynthesis or glycolysis was re-distributed into carbon-containing compounds, such as glucose-6-phosphate, fructose-6-phosphate, phosphoenolpyruvate, lactate, citrate, 3-hydroxybutyrate, and leucine, and then diverted into lipid metabolism for the production of storage lipids via the gamma-aminobutyrate pathway, glycolysis, and the tricarboxylic acid cycle. These results were substantiated in the model green alga Chlamydomonas reinhardtii by analyzing various mutants deficient in glutamate synthase/NADH-dependent, glutamate synthase/Fd-dependent, glutamine synthetase, aspartate aminotransferase, alanine aminotransferase, pyruvate kinase, and citrate synthase. Our study suggests that not only carbon but also nitrogen assimilation and distribution pathways contribute to lipid biosynthesis. Furthermore, these findings may facilitate genetic engineering efforts to enhance microalgal biofuel production.
Highlights
Biodiesel, one of the most commonly used biofuels, has attracted much attention as an ideal renewable energy carrier, and as a possible primary energy source [1]
Selection of three Chlorella strains with significant differences in lipid biosynthesis We determined the lipid contents of 15 Chlorella strains (Additional file 4: Figure S1) and identified three Chlorella strains, i.e., control stage (Cs). sorokiniana (C1), Chlorella sp. (C2), and C. sorokiniana (C3), that have significant differences in lipid productivity and a high level of nucleotide sequence identity in their 18S rRNA gene sequences [38]
Enhanced green fluorescence signals from Bodipy 505/515 were detected as time progressed in all three Chlorella strains, after 6 day of N starvation the strongest green fluorescence signal was observed in C2 and the weakest green fluorescence signal was detected in C3 (Fig. 1a, 6 day)
Summary
One of the most commonly used biofuels, has attracted much attention as an ideal renewable energy carrier, and as a possible primary energy source [1]. There has been renewed interest in producing biodiesel from microalgae, as microalgae can grow rapidly and convert solar energy into chemical energy via CO2 fixation. Using microalgae for environmental purposes (CO2 fixation, NOx, and wastewater treatment) has attracted much attention recently, and some environmental factors could induce lipid accumulation [4,5,6]. Microalgal metabolic pathways are heavily influenced by the environment [7]. Nitrogen (N) limitation and N starvation are primary factors that influence cell growth and metabolism, and these conditions may be used to enhance lipid biosynthesis in microalgae. When N is insufficient to support protein synthesis, excess carbon (C) from photosynthesis is diverted into storage molecules such as triglycerides and starch [8]
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