Deciphering the β-carotene hyperaccumulation in Dunaliella by the comprehensive analysis of Dunaliella salina and Dunaliella tertiolecta under high light conditions

Abstract

The green microalga Dunaliella salina hyperaccumulates β-carotene in the chloroplast, which turns its cells orange. This does not occur in the sister species Dunaliella tertiolecta. However, the molecular mechanisms of β-carotene hyperaccumulation were still unclear. Here, we discovered the reasons for β-carotene hyperaccumulation by comparing the morphology, physiology, genome, and transcriptome between the carotenogenic D. salina and the noncarotenogenic D. tertiolecta after transfer to high light. The differences in photosynthetic capacity, cell growth, and the concentration of stored carbon suggest that these species regulate the supply and utilization of carbon differently. The number of β-carotene-containing plastid lipid globules increased in both species, but much faster and to a greater extent in D. salina than in D. tertiolecta. Consistent with the accumulation of plastid lipid globules, the expression of the methyl-erythritol-phosphate and carotenoid biosynthetic pathways increased only in D. salina, which explains the de novo synthesis of β-carotene. In D. salina, the concomitantly upregulated expression of the carotene globule proteins suggests that hyperaccumulation of β-carotene also requires a simultaneous increase in its sink capacity. Based on genomic analysis, we propose that D. salina has genetic advantages for routing carbon from growth to carotenoid metabolism.