System metabolic tools reveal fucoxanthin metabolism in Nitzschia laevis for the improvement of fucoxanthin productivity

The production of fucoxanthin from microalgae is rapidly gaining popularity due to its exceptional productivity, lack of contamination, and straightforward extraction process. However, the optimal conditions for increasing biomass concentration and/or fucoxanthin content through the manipulation of light and carbon sources are context specific. This study explored fucoxanthin metabolism in Nitzschia laevis under heterotrophic and mixotrophic conditions using C-13 tracer-based metabolic flux analysis, targeted metabolomics, and transcriptome analysis. Mixotrophic culture at 10 mu mol m(-2) s(-1) improved fucoxanthin content by 27.54% but decreased biomass concentration by 15.65% compared to heterotrophic culture. At the molecular level, exposure to low light results in a reduction in carbon flux in the TCA cycle, leading to an increased flux toward carotenoid and fatty acid biosynthesis. The accumulation of high levels of citrate, isocitrate, and alpha-ketoglutaric acid is attributed to the reduced activity of the TCA cycle. Moreover, the metabolism of glyceraldehyde-3-phosphate and phosphoenolpyruvate was found to be more active under mixotrophic cultivation than heterotrophic ones, resulting in a substantial accumulation of fucoxanthin. The higher ATP and NADPH consumption provided sufficient energy for fucoxanthin and fatty acid biosynthesis. Furthermore, gene expression analysis revealed that low light upregulated the genes involved in fucoxanthin biosynthesis and promoted the violaxanthin cycle, especially after 12 h of cultivation. To improve fucoxanthin productivity, low light conditions were applied after a fed-batch culture, resulting in a 22.92% increase in fucoxanthin accumulation. The findings of this study offer valuable insights into the advantages of employing multi-stage cultivation techniques to improve microalgal production.

Automated summary

The production of fucoxanthin from microalgae is becoming popular due to its high productivity, lack of contamination, and simple extraction process. This study investigated the metabolism of fucoxanthin in Nitzschia laevis under different cultivation conditions and discovered that mixotrophic culture with low light conditions improved fucoxanthin content but decreased biomass concentration compared to heterotrophic culture. The study also revealed the molecular mechanisms behind the metabolic changes, including the redirection of carbon flux towards carotenoid and fatty acid synthesis and the upregulation of genes involved in fucoxanthin biosynthesis under low light conditions. These findings provide valuable insights into enhancing fucoxanthin production through multi-stage cultivation techniques.