Remodeling of the terpenoid metabolism during prolonged phosphate depletion in the marine diatom Phaeodactylum tricornutum

Abstract

Terpenoids are a diverse class of naturally occurring organic compounds, which derive from five-carbon isoprene units and play crucial roles in physiology, ecological interactions such as defense mechanisms, or adaptation to environmental stresses. In Phaeodactylum tricornutum, some of the most important isoprenoids are sterols and pigments, derived from precursors of the cytosolic mevalonate and the plastidial methyl-erythritol 4-phosphate pathway, respectively. However, the regulation of isoprenoid metabolism in P. tricornutum has not yet been characterized, presenting a major gap in our understanding of its ecological functions and adaptations. By leveraging metabolic, photosynthetic, and transcriptomic analyses, we characterized the dynamic remodeling of the isoprenoid pathways during prolonged nutrient stress in wild-type diatoms. We observed the down-regulation of the methylerythritol 4-phosphate and pigment biosynthesis pathways and the upregulation of key genes in the mevalonate and sterol biosynthesis pathways. At the metabolite level, we observed an overall decrease in pigment and no changes in sterol levels. Using a genetically engineered diatom strain to produce a heterologous monoterpenoid to monitor the availability of one of the main terpenoid precursors, geranyl diphosphate (GPP), we suggest that cytosolic GPP pools increase during prolonged phosphate depletion. Our results have demonstrated how the biosynthesis of isoprenoid metabolites and the pools of prenyl phosphate are vastly remodeled during phosphate depletion. We anticipate that the knowledge generated in this study can serve as a foundation for understanding ecological responses and adaptations of diatoms to nutrient stress, contributing to our broader comprehension of marine ecosystem dynamics and design strategies for producing high-value compounds in diatoms.