Methyl jasmonate treatment affects the regulation of the 2-C-methyl-D-erythritol 4-phosphate pathway and early steps of the triterpenoid biosynthesis in Chlamydomonas reinhardtii

Abstract

Terpenoids are a large and diverse class of naturally occurring metabolites serving many industrial applications and natural roles. Economically important terpenoids are often produced in low abundance from their natural sources, making their industrial-scale production challenging or uneconomical, therefore engineered microorganisms are frequently used as heterologous production platforms. Photosynthetic microorganisms, such as the green alga Chlamydomonas reinhardtii, represent promising systems to produce terpenoids in a cost-effective and sustainable manner, but knowledge about the regulation of their terpenoid metabolism remains limited. Here we report on the investigation of the phytohormone methyl jasmonate (MeJA) as elicitor of algal terpenoid synthesis. We treated C. reinhardtii cells in mid-exponential growth phase with three different concentrations of MeJA (0.05, 0.5 and 1 mM). The highest concentration of MeJA affected the photosynthetic activity of the cells, arrested the growth and up-regulated key genes of the 2-C-methyl-D-erythritol 4-phosphate (MEP) pathway, leading to a significant increase in intermediates of this pathway, squalene and (S)-2,3-epoxysqualene, while the abundance of cycloartenol, and two main sterols (ergosterol and 7-dehydroporiferasterol) decreased. These data suggest the redirection of the carbon flux towards the synthesis of yet uncharacterised triterpenoid secondary metabolites upon MeJA treatment. Our results offer important new insights into the regulation of the triterpenoid metabolism in C. reinhardtii and raise important questions on hormonal signalling in microalgae. Phytohormone treatment is tested for the first time in algae, where it holds great potential for identifying key transcriptional regulators of the MEP pathway as targets for future metabolic engineering studies for improve production of high-value triterpenoids.