An unexpected hydratase synthesizes the green light-absorbing pigment fucoxanthin

Cao, Tianjun; Bai, Yu; Buschbeck, Paul; Tan, Qiaozhu; Cantrell, Michael B.; Chen, Yinjuan; Jiang, Yanyou; Liu, Run-Zhou; Ries, Nana K.; Shi, Xiaohuo; Sun, Yan; Ware, Maxwell A.; Yang, Fenghua; Zhang, Huan; Han, Jichang; Zhang, Lihan; Huang, Jing; Lohr, Martin; Peers, Graham; Li, Xiaobo

doi:10.1093/plcell/koad116

An unexpected hydratase synthesizes the green light-absorbing pigment fucoxanthin

Journal Article · Wed Apr 26 04:00:00 EDT 2023 · The Plant Cell

DOI:https://doi.org/10.1093/plcell/koad116· OSTI ID:2420770

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OSTI

Abstract

The ketocarotenoid fucoxanthin and its derivatives can absorb blue–green light enriched in marine environments. Fucoxanthin is widely adopted by phytoplankton species as a main light-harvesting pigment, in contrast to land plants that primarily employ chlorophylls. Despite its supreme abundance in the oceans, the last steps of fucoxanthin biosynthesis have remained elusive. Here, we identified the carotenoid isomerase-like protein CRTISO5 as the diatom fucoxanthin synthase that is related to the carotenoid cis–trans isomerase CRTISO from land plants but harbors unexpected enzymatic activity. A crtiso5 knockout mutant in the model diatom Phaeodactylum tricornutum completely lacked fucoxanthin and accumulated the acetylenic carotenoid phaneroxanthin. Recombinant CRTISO5 converted phaneroxanthin into fucoxanthin in vitro by hydrating its carbon–carbon triple bond, instead of functioning as an isomerase. Molecular docking and mutational analyses revealed residues essential for this activity. Furthermore, a photophysiological characterization of the crtiso5 mutant revealed a major structural and functional role of fucoxanthin in photosynthetic pigment–protein complexes of diatoms. As CRTISO5 hydrates an internal alkyne physiologically, the enzyme has unique potential for biocatalytic applications. The discovery of CRTISO5 illustrates how neofunctionalization leads to major diversification events in evolution of photosynthetic mechanisms and the prominent brown coloration of most marine photosynthetic eukaryotes.

Research Organization:: J. Craig Venter Institute, Inc., Rockville, MD (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: SC0018344

OSTI ID:: 2420770

Journal Information:: The Plant Cell, Journal Name: The Plant Cell Journal Issue: 8 Vol. 35; ISSN 1040-4651

Publisher:: American Society of Plant Biologists (ASPB)

Country of Publication:: United States

Language:: English

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