Aureochromes maintain polyunsaturated fatty acid content in Nannochloropsis oceanica

Poliner, Eric; Busch, Andrea W. U.; Newton, Linsey; Kim, Young Uk; Clark, Rachel; Gonzalez-Martinez, Sofía C.; Jeong, Byeong-Ryool; Montgomery, Beronda L.; Farré, Eva M.

doi:10.1093/plphys/kiac052

Aureochromes maintain polyunsaturated fatty acid content in Nannochloropsis oceanica

Journal Article · 15 February 2022 · Plant Physiology (Bethesda)

DOI:https://doi.org/10.1093/plphys/kiac052· OSTI ID:1979586

; Busch, Andrea W. U.; ; Kim, Young Uk; ; Gonzalez-Martinez, Sofía C.; ; ;

Abstract Nannochloropsis oceanica, like other stramenopile microalgae, is rich in long-chain polyunsaturated fatty acids (LC-PUFAs) such as eicosapentaenoic acid (EPA). We observed that fatty acid desaturases (FADs) involved in LC-PUFA biosynthesis were among the strongest blue light-induced genes in N. oceanica CCMP1779. Blue light was also necessary for maintaining LC-PUFA levels in CCMP1779 cells, and growth under red light led to a reduction in EPA content. Aureochromes are stramenopile-specific proteins that contain a light–oxygen–voltage (LOV)-sensing domain that associates with a flavin mononucleotide and is able to sense blue light. These proteins also contain a basic leucine zipper DNA-binding motif and can act as blue light-regulated transcription factors by associating with an E-box like motif, which we found enriched in the promoters of blue light-induced genes. We demonstrated that, in vitro, two CCMP1779 aureochromes were able to absorb blue light. Moreover, the loss or reduction of the expression of any of the three aureochrome genes led to a decrease in the blue light-specific induction of several FADs in CCMP1779. EPA content was also significantly reduced in NoAUREO2 and NoAUREO4 mutants. Taken together, our results indicate that aureochromes mediate blue light-dependent regulation of LC-PUFA content in N. oceanica CCMP1779 cells.

Research Organization:: Michigan State Univ., East Lansing, MI (United States)

Sponsoring Organization:: USDOE Office of Science (SC)

DOE Contract Number:: FG02-91ER20021

OSTI ID:: 1979586

Journal Information:: Plant Physiology (Bethesda), Vol. 189, Issue 2; ISSN 0032-0889

Publisher:: American Society of Plant Biologists

Country of Publication:: United States

Language:: English

References (55)

Towards sustainable sources for omega-3 fatty acids production Adarme-Vega, T. Catalina; Thomas-Hall, Skye R.; Schenk, Peer M. Current Opinion in Biotechnology, Vol. 26 https://doi.org/10.1016/j.copbio.2013.08.003	journal	April 2014
Light Remodels Lipid Biosynthesis in Nannochloropsis gaditana by Modulating Carbon Partitioning between Organelles Alboresi, Alessandro; Perin, Giorgio; Vitulo, Nicola Plant Physiology, Vol. 171, Issue 4 https://doi.org/10.1104/pp.16.00599	journal	June 2016
Neighbour signals perceived by phytochrome B increase thermotolerance in Arabidopsis Arico, Denise; Legris, Martina; Castro, Luciana Plant, Cell & Environment, Vol. 42, Issue 9 https://doi.org/10.1111/pce.13575	journal	May 2019
Allosteric communication between DNA-binding and light-responsive domains of diatom class I aureochromes Banerjee, Ankan; Herman, Elena; Serif, Manuel Nucleic Acids Research, Vol. 44, Issue 12 https://doi.org/10.1093/nar/gkw420	journal	May 2016
The diurnal transcriptional landscape of the microalga Tetradesmus obliquus Carreres, Benoit M.; León-Saiki, G. Mitsue; Schaap, Peter J. Algal Research, Vol. 40 https://doi.org/10.1016/j.algal.2019.101477	journal	June 2019
Gene Regulation of Carbon Fixation, Storage, and Utilization in the Diatom Phaeodactylum tricornutum Acclimated to Light/Dark Cycles Chauton, Matilde Skogen; Winge, Per; Brembu, Tore Plant Physiology, Vol. 161, Issue 2 https://doi.org/10.1104/pp.112.206177	journal	December 2012
Enhancing the production of eicosapentaenoic acid (EPA) from Nannochloropsis oceanica CY2 using innovative photobioreactors with optimal light source arrangements Chen, Chun-Yen; Chen, Yu-Chun; Huang, Hsiao-Chen Bioresource Technology, Vol. 191 https://doi.org/10.1016/j.biortech.2015.03.001	journal	September 2015
Engineering strategies for enhancing the production of eicosapentaenoic acid (EPA) from an isolated microalga Nannochloropsis oceanica CY2 Chen, Chun-Yen; Chen, Yu-Chun; Huang, Hsiao-Chen Bioresource Technology, Vol. 147 https://doi.org/10.1016/j.biortech.2013.08.051	journal	November 2013
Diatom PtCPF1 is a new cryptochrome/photolyase family member with DNA repair and transcription regulation activity Coesel, Sacha; Mangogna, Manuela; Ishikawa, Tomoko EMBO reports, Vol. 10, Issue 6 https://doi.org/10.1038/embor.2009.59	journal	May 2009
Enhanced algae growth in both phototrophic and mixotrophic culture under blue light Das, Probir; Lei, Wang; Aziz, Siti Sarah Bioresource Technology, Vol. 102, Issue 4 https://doi.org/10.1016/j.biortech.2010.11.102	journal	February 2011
Genomic determinants of coral heat tolerance across latitudes Dixon, Groves B.; Davies, Sarah W.; Aglyamova, Galina V. Science, Vol. 348, Issue 6242 https://doi.org/10.1126/science.1261224	journal	June 2015
Marine algae and land plants share conserved phytochrome signaling systems Duanmu, D.; Bachy, C.; Sudek, S. Proceedings of the National Academy of Sciences, Vol. 111, Issue 44 https://doi.org/10.1073/pnas.1416751111	journal	September 2014
Algal light sensing and photoacclimation in aquatic environments: Bilin and light signalling in eukaryotic algae Duanmu, Deqiang; Rockwell, Nathan C.; Lagarias, J. Clark Plant, Cell & Environment, Vol. 40, Issue 11 https://doi.org/10.1111/pce.12943	journal	May 2017
Gene Expression Omnibus: NCBI gene expression and hybridization array data repository Edgar, R. Nucleic Acids Research, Vol. 30, Issue 1 https://doi.org/10.1093/nar/30.1.207	journal	January 2002
Structural and evolutionary aspects of algal blue light receptors of the cryptochrome and aureochrome type Essen, Lars-Oliver; Franz, Sophie; Banerjee, Ankan Journal of Plant Physiology, Vol. 217 https://doi.org/10.1016/j.jplph.2017.07.005	journal	October 2017
Observations on the Diversity and Ecology of Freshwater Nannochloropsis (Eustigmatophyceae), with Descriptions of New Taxa Fawley, Karen P.; Fawley, Marvin W. Protist, Vol. 158, Issue 3 https://doi.org/10.1016/j.protis.2007.03.003	journal	July 2007
Diatom Phytochromes Reveal the Existence of Far-Red-Light-Based Sensing in the Ocean Fortunato, Antonio Emidio; Jaubert, Marianne; Enomoto, Gen The Plant Cell, Vol. 28, Issue 3 https://doi.org/10.1105/tpc.15.00928	journal	March 2016
Blue light-induced LOV domain dimerization enhances the affinity of Aureochrome 1a for its target DNA sequence Heintz, Udo; Schlichting, Ilme eLife, Vol. 5 https://doi.org/10.7554/eLife.11860	journal	January 2016
Simple Combinations of Lineage-Determining Transcription Factors Prime cis-Regulatory Elements Required for Macrophage and B Cell Identities Heinz, Sven; Benner, Christopher; Spann, Nathanael Molecular Cell, Vol. 38, Issue 4 https://doi.org/10.1016/j.molcel.2010.05.004	journal	May 2010
Blue Light-Induced Conformational Changes in a Light-Regulated Transcription Factor, Aureochrome-1 Hisatomi, Osamu; Takeuchi, Ken; Zikihara, Kazunori Plant and Cell Physiology, Vol. 54, Issue 1 https://doi.org/10.1093/pcp/pcs160	journal	December 2012
AUREOCHROME1a-Mediated Induction of the Diatom-Specific Cyclin dsCYC2 Controls the Onset of Cell Division in Diatoms ( Phaeodactylum tricornutum ) Huysman, Marie J. J.; Fortunato, Antonio E.; Matthijs, Michiel The Plant Cell, Vol. 25, Issue 1 https://doi.org/10.1105/tpc.112.106377	journal	January 2013
Dynamic Light Regulation of Translation Status in Arabidopsis thaliana Juntawong, Piyada; Bailey-Serres, Julia Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00066	journal	January 2012
Light-induced expression of fatty acid desaturase genes Kis, Mihály; Zsiros, Otto; Farkas, Tibor Proceedings of the National Academy of Sciences, Vol. 95, Issue 8 https://doi.org/10.1073/pnas.95.8.4209	journal	April 1998
An update on aureochromes: Phylogeny – mechanism – function Kroth, Peter G.; Wilhelm, Christian; Kottke, Tilman Journal of Plant Physiology, Vol. 217 https://doi.org/10.1016/j.jplph.2017.06.010	journal	October 2017
MEGA X: Molecular Evolutionary Genetics Analysis across Computing Platforms Kumar, Sudhir; Stecher, Glen; Li, Michael Molecular Biology and Evolution, Vol. 35, Issue 6 https://doi.org/10.1093/molbev/msy096	journal	May 2018
The lipid biochemistry of eukaryotic algae Li-Beisson, Yonghua; Thelen, Jay J.; Fedosejevs, Eric Progress in Lipid Research, Vol. 74 https://doi.org/10.1016/j.plipres.2019.01.003	journal	April 2019
Triacylglycerol profiling of microalgae Chlamydomonas reinhardtii and Nannochloropsis oceanica Liu, Bensheng; Vieler, Astrid; Li, Chao Bioresource Technology, Vol. 146 https://doi.org/10.1016/j.biortech.2013.07.088	journal	October 2013
Extension of a genetic network model by iterative experimentation and mathematical analysis Locke, James C. W.; Southern, Megan M.; Kozma‐Bognár, László Molecular Systems Biology, Vol. 1, Issue 1 https://doi.org/10.1038/msb4100018	journal	January 2005
PtAUREO1a and PtAUREO1b knockout mutants of the diatom Phaeodactylum tricornutum are blocked in photoacclimation to blue light Mann, Marcus; Serif, Manuel; Jakob, Torsten Journal of Plant Physiology, Vol. 217 https://doi.org/10.1016/j.jplph.2017.05.020	journal	October 2017
The Aureochrome Photoreceptor PtAUREO1a Is a Highly Effective Blue Light Switch in Diatoms Mann, Marcus; Serif, Manuel; Wrobel, Thomas iScience, Vol. 23, Issue 11 https://doi.org/10.1016/j.isci.2020.101730	journal	November 2020
Translation regulation in plants: an interesting past, an exciting present and a promising future Merchante, Catharina; Stepanova, Anna N.; Alonso, Jose M. The Plant Journal, Vol. 90, Issue 4 https://doi.org/10.1111/tpj.13520	journal	March 2017
Network Discovery Pipeline Elucidates Conserved Time-of-Day–Specific cis-Regulatory Modules Michael, Todd P.; Mockler, Todd C.; Breton, Ghislain PLoS Genetics, Vol. 4, Issue 2 https://doi.org/10.1371/journal.pgen.0040014	journal	January 2008
NLStradamus: a simple Hidden Markov Model for nuclear localization signal prediction Nguyen Ba, Alex N.; Pogoutse, Anastassia; Provart, Nicholas BMC Bioinformatics, Vol. 10, Issue 1 https://doi.org/10.1186/1471-2105-10-202	journal	January 2009
A high-capacity gene stacking toolkit for the oleaginous microalga, Nannochloropsis oceanica CCMP1779 Poliner, Eric; Clark, Evan; Cummings, Cameron Algal Research, Vol. 45 https://doi.org/10.1016/j.algal.2019.101664	journal	January 2020
Advanced genetic tools enable synthetic biology in the oleaginous microalgae Nannochloropsis sp. Poliner, Eric; Farré, Eva M.; Benning, Christoph Plant Cell Reports, Vol. 37, Issue 10 https://doi.org/10.1007/s00299-018-2270-0	journal	March 2018
Transcriptional coordination of physiological responses in Nannochloropsis oceanica CCMP1779 under light/dark cycles Poliner, Eric; Panchy, Nicholas; Newton, Linsey The Plant Journal, Vol. 83, Issue 6 https://doi.org/10.1111/tpj.12944	journal	August 2015
A toolkit for Nannochloropsis oceanica CCMP1779 enables gene stacking and genetic engineering of the eicosapentaenoic acid pathway for enhanced long-chain polyunsaturated fatty acid production Poliner, Eric; Pulman, Jane A.; Zienkiewicz, Krzysztof Plant Biotechnology Journal, Vol. 16, Issue 1 https://doi.org/10.1111/pbi.12772	journal	July 2017
Nontransgenic Marker-Free Gene Disruption by an Episomal CRISPR System in the Oleaginous Microalga, Nannochloropsis oceanica CCMP1779 Poliner, Eric; Takeuchi, Tomomi; Du, Zhi-Yan ACS Synthetic Biology, Vol. 7, Issue 4 https://doi.org/10.1021/acssynbio.7b00362	journal	March 2018
Diel oscillation in the optical activity of carotenoids in the absorption spectrum of Nannochloropsis Possa, Gabriela C.; Santana, Hugo; Brasil, Bruno S. A. F. Journal of Molecular Modeling, Vol. 23, Issue 3 https://doi.org/10.1007/s00894-017-3268-1	journal	February 2017
Light as an information carrier underwater Ragni, M. Journal of Plankton Research, Vol. 26, Issue 4 https://doi.org/10.1093/plankt/fbh044	journal	February 2004
Phytochrome evolution in 3D: deletion, duplication, and diversification Rockwell, Nathan C.; Lagarias, J. Clark New Phytologist, Vol. 225, Issue 6 https://doi.org/10.1111/nph.16240	journal	November 2019
Plant Responses to Vegetation Proximity: A Whole Life Avoiding Shade Roig-Villanova, Irma; Martínez-García, Jaime F. Frontiers in Plant Science, Vol. 7 https://doi.org/10.3389/fpls.2016.00236	journal	February 2016
Modulation of lipid biosynthesis by stress in diatoms Sayanova, Olga; Mimouni, Virginie; Ulmann, Lionel Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728 https://doi.org/10.1098/rstb.2016.0407	journal	July 2017
Aureochrome 1a Is Involved in the Photoacclimation of the Diatom Phaeodactylum tricornutum Schellenberger Costa, Benjamin; Sachse, Matthias; Jungandreas, Anne PLoS ONE, Vol. 8, Issue 9 https://doi.org/10.1371/journal.pone.0074451	journal	September 2013
Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation Smith, Sarah R.; Gillard, Jeroen T. F.; Kustka, Adam B. PLOS Genetics, Vol. 12, Issue 12 https://doi.org/10.1371/journal.pgen.1006490	journal	December 2016
Molecular Evolutionary Genetics Analysis (MEGA) for macOS Stecher, Glen; Tamura, Koichiro; Kumar, Sudhir Molecular Biology and Evolution, Vol. 37, Issue 4 https://doi.org/10.1093/molbev/msz312	journal	January 2020
Photosynthetic performance of outdoor Nannochloropsis mass cultures under a wide range of environmental conditions Sukenik, A.; Beardall, J.; Kromkamp, Jc Aquatic Microbial Ecology, Vol. 56 https://doi.org/10.3354/ame01309	journal	September 2009
Regulation of Fatty acid Composition by Irradiance Level in the Eustigmatophyte Nannochloropsis sp.1 Sukenik, Assaf; Carmeli, Yael; Berner, Tamar Journal of Phycology, Vol. 25, Issue 4 https://doi.org/10.1111/j.0022-3646.1989.00686.x	journal	December 1989
AUREOCHROME, a photoreceptor required for photomorphogenesis in stramenopiles Takahashi, F.; Yamagata, D.; Ishikawa, M. Proceedings of the National Academy of Sciences, Vol. 104, Issue 49 https://doi.org/10.1073/pnas.0707692104	journal	November 2007
Light and the circadian clock mediate time-specific changes in sensitivity to UV-B stress under light/dark cycles Takeuchi, Tomomi; Newton, Linsey; Burkhardt, Alyssa Journal of Experimental Botany, Vol. 65, Issue 20 https://doi.org/10.1093/jxb/eru339	journal	August 2014
Photoreactions of Aureochrome-1 Toyooka, Tsuguyoshi; Hisatomi, Osamu; Takahashi, Fumio Biophysical Journal, Vol. 100, Issue 11 https://doi.org/10.1016/j.bpj.2011.02.043	journal	June 2011
Green microalgae in marine coastal waters: The Ocean Sampling Day (OSD) dataset Tragin, Margot; Vaulot, Daniel Scientific Reports, Vol. 8, Issue 1 https://doi.org/10.1038/s41598-018-32338-w	journal	September 2018
Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks Trapnell, Cole; Roberts, Adam; Goff, Loyal Nature Protocols, Vol. 7, Issue 3 https://doi.org/10.1038/nprot.2012.016	journal	March 2012
Genome, Functional Gene Annotation, and Nuclear Transformation of the Heterokont Oleaginous Alga Nannochloropsis oceanica CCMP1779 Vieler, Astrid; Wu, Guangxi; Tsai, Chia-Hong PLoS Genetics, Vol. 8, Issue 11 https://doi.org/10.1371/journal.pgen.1003064	journal	November 2012
Nannochloropsis Genomes Reveal Evolution of Microalgal Oleaginous Traits Wang, Dongmei; Ning, Kang; Li, Jing PLoS Genetics, Vol. 10, Issue 1 https://doi.org/10.1371/journal.pgen.1004094	journal	January 2014

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