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Title: An algal enzyme required for biosynthesis of the most abundant marine carotenoids

Abstract

Fucoxanthin and its derivatives are the main light-harvesting pigments in the photosynthetic apparatus of many chromalveolate algae and represent the most abundant carotenoids in the world’s oceans, thus being major facilitators of marine primary production. A central step in fucoxanthin biosynthesis that has been elusive so far is the conversion of violaxanthin to neoxanthin. Here, we show that in chromalveolates, this reaction is catalyzed by violaxanthin de-epoxidase–like (VDL) proteins and that VDL is also involved in the formation of other light-harvesting carotenoids such as peridinin or vaucheriaxanthin. VDL is closely related to the photoprotective enzyme violaxanthin de-epoxidase that operates in plants and most algae, revealing that in major phyla of marine algae, an ancient gene duplication triggered the evolution of carotenoid functions beyond photoprotection toward light harvesting.

Authors:
ORCiD logo [1]; ORCiD logo [2]; ORCiD logo [3]; ORCiD logo [4]; ORCiD logo [4];  [4]; ORCiD logo [4]; ORCiD logo [4];  [4];  [4]; ORCiD logo [3]; ORCiD logo [5]; ORCiD logo [4]
+ Show Author Affiliations
  1. Johannes Gutenberg Univ., Mainz (Germany). Inst. für Molekulare Physiologie, Pflanzenbiochemi
  2. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States)
  3. Univ. of California, Berkeley, CA (United States)
  4. Johannes Gutenberg Univ., Mainz (Germany). Inst. für Molekulare Physiologie, Pflanzenbiochemi
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States); Univ. of California, Berkeley, CA (United States). Howard Hughes Medical Inst.
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences, and Biosciences Division; Danish Council for Independent Research
OSTI Identifier:
1609117
Grant/Contract Number:  
AC02-05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Science Advances
Additional Journal Information:
Journal Volume: 6; Journal Issue: 10; Journal ID: ISSN 2375-2548
Publisher:
AAAS
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Dautermann, O., Lyska, D., Andersen-Ranberg, J., Becker, M., Fröhlich-Nowoisky, J., Gartmann, H., Krämer, L. C., Mayr, K., Pieper, D., Rij, L. M., Wipf, H. M. -L., Niyogi, K. K., and Lohr, M. An algal enzyme required for biosynthesis of the most abundant marine carotenoids. United States: N. p., 2020. Web. doi:10.1126/sciadv.aaw9183.
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Dautermann, O., Lyska, D., Andersen-Ranberg, J., Becker, M., Fröhlich-Nowoisky, J., Gartmann, H., Krämer, L. C., Mayr, K., Pieper, D., Rij, L. M., Wipf, H. M. -L., Niyogi, K. K., & Lohr, M. An algal enzyme required for biosynthesis of the most abundant marine carotenoids. United States. https://doi.org/10.1126/sciadv.aaw9183
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Dautermann, O., Lyska, D., Andersen-Ranberg, J., Becker, M., Fröhlich-Nowoisky, J., Gartmann, H., Krämer, L. C., Mayr, K., Pieper, D., Rij, L. M., Wipf, H. M. -L., Niyogi, K. K., and Lohr, M. Wed . "An algal enzyme required for biosynthesis of the most abundant marine carotenoids". United States. https://doi.org/10.1126/sciadv.aaw9183. https://www.osti.gov/servlets/purl/1609117.
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@article{osti_1609117,
title = {An algal enzyme required for biosynthesis of the most abundant marine carotenoids},
author = {Dautermann, O. and Lyska, D. and Andersen-Ranberg, J. and Becker, M. and Fröhlich-Nowoisky, J. and Gartmann, H. and Krämer, L. C. and Mayr, K. and Pieper, D. and Rij, L. M. and Wipf, H. M. -L. and Niyogi, K. K. and Lohr, M.},
abstractNote = {Fucoxanthin and its derivatives are the main light-harvesting pigments in the photosynthetic apparatus of many chromalveolate algae and represent the most abundant carotenoids in the world’s oceans, thus being major facilitators of marine primary production. A central step in fucoxanthin biosynthesis that has been elusive so far is the conversion of violaxanthin to neoxanthin. Here, we show that in chromalveolates, this reaction is catalyzed by violaxanthin de-epoxidase–like (VDL) proteins and that VDL is also involved in the formation of other light-harvesting carotenoids such as peridinin or vaucheriaxanthin. VDL is closely related to the photoprotective enzyme violaxanthin de-epoxidase that operates in plants and most algae, revealing that in major phyla of marine algae, an ancient gene duplication triggered the evolution of carotenoid functions beyond photoprotection toward light harvesting.},
doi = {10.1126/sciadv.aaw9183},
journal = {Science Advances},
number = 10,
volume = 6,
place = {United States},
year = {Wed Mar 04 00:00:00 EST 2020},
month = {Wed Mar 04 00:00:00 EST 2020}
}
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Journal Article:
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https://doi.org/10.1126/sciadv.aaw9183
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Cited by: 31 works
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Figures / Tables:

Fig. 1 Fig. 1: A vdl knockout mutant of N. oceanica no longer synthesizes the allenic vaucheriaxanthin acyl esters. (A) HPLC analyses (system IIb) of pigment extracts from wild type, the vdl mutant, and a vdl mutant complemented with its native VDL gene (vdl + VDL, clone #4) demonstrate that knockout ofmore » the VDL gene results in loss of vaucheriaxanthin acyl esters (peaks 3 and 4) and a concomitant increase in violaxanthin (2). Chromatograms were normalized to chlorophyll a (5); other peaks were identified as latoxanthin (1) and β-carotene (6). For detailed pigment stoichiometries in the wild type, the vdl mutant, and two VDL-complemented strains of the vdl mutant, see table S1. (B) Scheme showing the insertion site of the 1.8-kb zeocin resistance cassette (ZeoR) within the second exon of the VDL gene in the vdl mutant. Binding sites of the primers used for differentiation of wild-type (WT) and mutated VDL gene are indicated by black arrows. (C) Agarose gel showing 1.8-kb size difference of polymerase chain reaction (PCR) products of WT or the VDL-deficient mutant (vdl) using PCR primers specified in (B). (D) Agarose gel showing additional band of WT VDL fragment at 1.4 kb for PCR products from successfully complemented transformants of the vdl mutant; clones #2 and #4 were used for pigment analyses. Other experimental details are described in Materials and Methods.« less
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