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

J Agric Food Chem. 2020 Feb 5;68(5):1354-1363. doi: 10.1021/acs.jafc.9b06918. Epub 2020 Jan 27.

Abstract

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.

Keywords: Porphyra umbilicalis; Pyropia yezoensis; carotenoid; evolution; lutein; lycopene; lycopene cyclase; red algae.

MeSH terms

  • 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

Substances

  • Plant Proteins
  • Intramolecular Lyases
  • lycopene cyclase-isomerase
  • Lycopene
  • Lutein