Green diatom mutants reveal an intricate biosynthetic pathway of fucoxanthin

Bai, Yu; Cao, Tianjun; Dautermann, Oliver; Buschbeck, Paul; Cantrell, Michael B.; Chen, Yinjuan; Lein, Christopher D.; Shi, Xiaohuo; Ware, Maxwell A.; Yang, Fenghua; Zhang, Huan; Zhang, Lihan; Peers, Graham; Li, Xiaobo; Lohr, Martin

doi:10.1073/pnas.2203708119

Green diatom mutants reveal an intricate biosynthetic pathway of fucoxanthin

Journal Article · Mon Sep 12 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2203708119· OSTI ID:1886753

^[1]; ^[2]; ^[3]; ^[3]; ^[1]; Chen, Yinjuan ^[4]; Lein, Christopher D. ^[3]; Shi, Xiaohuo ^[4]; Ware, Maxwell A. ^[1]; Yang, Fenghua ^[5]; Zhang, Huan ^[2]; ^[6]; ^[1]; ^[2]; ^[3]

Department of Biology, Colorado State University, Fort Collins, CO 80523-1878
Key Laboratory of Growth Regulation and Translational Research of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou 310024, China, Institute of Biology, Westlake Institute for Advanced Study, Hangzhou 310024, China
Institut für Molekulare Physiologie, Johannes Gutenberg-Universität, 55099 Mainz, Germany
Key Laboratory of Precise Synthesis of Functional Molecules of Zhejiang Province, School of Science, Instrumentation and Service Center for Molecular Sciences, Westlake University, Hangzhou 310024, China
Key Laboratory of Structural Biology of Zhejiang Province, School of Life Sciences, Westlake University, Hangzhou 310024, China
Key Laboratory of Precise Synthesis of Functional Molecules of Zhejiang Province, School of Science, Westlake University, Hangzhou 310024, China, Institute of Natural Sciences, Westlake Institute for Advanced Study, Hangzhou 310024, China.

Fucoxanthin is a major light-harvesting pigment in ecologically important algae such as diatoms, haptophytes, and brown algae (Phaeophyceae). Therefore, it is a major driver of global primary productivity. Species of these algal groups are brown colored because the high amounts of fucoxanthin bound to the proteins of their photosynthetic machineries enable efficient absorption of green light. While the structure of these fucoxanthin-chlorophyll proteins has recently been resolved, the biosynthetic pathway of fucoxanthin is still unknown. Here, we identified two enzymes central to this pathway by generating corresponding knockout mutants of the diatom Phaeodactylum tricornutum that are green due to the lack of fucoxanthin. Complementation of the mutants with the native genes or orthologs from haptophytes restored fucoxanthin biosynthesis. We propose a complete biosynthetic path to fucoxanthin in diatoms and haptophytes based on the carotenoid intermediates identified in the mutants and in vitro biochemical assays. It is substantially more complex than anticipated and reveals diadinoxanthin metabolism as the central regulatory hub connecting the photoprotective xanthophyll cycle and the formation of fucoxanthin. Moreover, our data show that the pathway evolved by repeated duplication and neofunctionalization of genes for the xanthophyll cycle enzymes violaxanthin de-epoxidase and zeaxanthin epoxidase. Brown algae lack diadinoxanthin and the genes described here and instead use an alternative pathway predicted to involve fewer enzymes. Our work represents a major step forward in elucidating the biosynthesis of fucoxanthin and understanding the evolution, biogenesis, and regulation of the photosynthetic machinery in algae.

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Research Organization:: Colorado State University, Fort Collins, CO (United States); J. Craig Venter Institute, Inc., Rockville, MD (United States)

Sponsoring Organization:: China Postdoctoral Science Foundation; National Key R&D Program of China; USDOE; USDOE Office of Science (SC), Biological and Environmental Research (BER); Westlake Education Foundation

Grant/Contract Number:: SC0018344

OSTI ID:: 1886753

Alternate ID(s):: OSTI ID: 1979176

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 38 Vol. 119; ISSN 0027-8424

Publisher:: Proceedings of the National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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