Functional Characterization of Lycopene Cyclases Illustrates the Metabolic Pathway toward Lutein in Red Algal Seaweeds

• Published in: Journal of agricultural and food chemistry 2020-02, Vol.68 (5), p.1354-1363
• Main Authors: Deng, Yin-Yin, Cheng, Lu, Wang, Qi, Ge, Zi-Han, Zheng, Hui, Cao, Tian-Jun, Lu, Qin-Qin, Yang, Li-En, Lu, Shan
• Format: Article
• Language: English
• Subjects: Amino Acid Sequence; Intramolecular Lyases - chemistry; Intramolecular Lyases - genetics; Intramolecular Lyases - metabolism; Lutein - chemistry; Lutein - metabolism; Lycopene - chemistry; Lycopene - metabolism; Phylogeny; Plant Proteins - chemistry; Plant Proteins - genetics; Plant Proteins - metabolism; Rhodophyta - classification; Rhodophyta - enzymology; Rhodophyta - genetics; Rhodophyta - metabolism; Seaweed - classification; Seaweed - enzymology; Seaweed - genetics; Seaweed - metabolism; Sequence Alignment
• ISSN: 0021-8561; 1520-5118
• DOI: 10.1021/acs.jafc.9b06918

Carotenoids are essential phytonutrients synthesized by all photosynthetic organisms. Acyclic lycopene is the first branching point for carotenoid biosynthesis. Lycopene β- and ε-cyclases (LCYB and LCYE, respectively) catalyze the cyclization of its open ends and direct the metabolic flux into different downstream branches. Carotenoids of the β,β-branch (e.g., β-carotene) are found in all photosynthetic organisms, but those of the β,ε-branch (e.g., lutein) are generally absent in cyanobacteria, heterokonts, and some red algae. Although both LCYBs and LCYEs have been characterized from land plants, there are only a few reports on LCYs from cyanobacteria and algae. Here, we cloned four LCY genes from Porphyra umbilicalis and Pyropia yezoensis (susabi-nori) of Bangiales, the most primitive red algal order that synthesizes lutein. Our functional characterization in both Escherichia coli and Arabidopsis thaliana demonstrated that each species has a pair of LCYB and LCYE. Similar to LCYs from higher plants, red algal LCYBs cyclize both ends of lycopene, and their LCYEs only cyclize a single end. The characterization of LCYEs from red algae resolved the first bifurcation step toward β-carotene and lutein biosynthesis. Our phylogenetic analysis suggests that LCYEs of the green lineage and the red algae originated separately during evolution.