High light boosts salinity stress-induced biosynthesis of astaxanthin and lipids in the green alga Chromochloris zofingiensis

Abstract

Chromochloris zofingiensis, an astaxanthin-producing oleaginous green alga, is emerging as a model for studying carotenogenesis and lipogenesis. While the stimulated biosynthesis of secondary carotenoids and storage lipids by abiotic stresses has long been perceived in C. zofingiensis, the underlying mechanisms particularly under combinatorial stresses remain to be explored. In the present study, the synthesis of carotenoids and lipids was comparatively investigated in C. zofingiensis under high light (HL), salinity stress (SS) and the combinatorial HL and SS (HL + SS) conditions. While HL or SS alone enhanced astaxanthin and lipids moderately, HL + SS had synergistic effect and promoted these compounds considerably. HL + SS also gave rise to the highest productivities. Carotenoid profiling and transcriptional analysis supported the diversion of carotenoid flux from primary carotenoids to secondary carotenoids particularly astaxanthin and violaxanthin cycle that produces zeaxanthin likely contributed to astaxanthin synthesis. Lipid profiling and transcriptional analysis, on the other hand, suggested that both de novo fatty acid synthesis and membrane lipid turnover contributed fatty acyls for supporting triacylglycerol assembly via the acyl CoA-dependent and acyl CoA-independent routes. Astaxanthin and triacylglycerol that share common carbon precursors were induced to synthesize in a coordinated way regulated at the transcriptional level, yet the carbon flux was allocated predominantly to the latter. Taken together, our results demonstrated the beneficial effect of combinatorial stresses on both astaxanthin and triacylglycerol production, identified critical genes involved in carotenogenesis and lipogenesis, and provided new insights into algal astaxanthin biosynthesis.