Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom

Sarah R. Smith, Chris L. Dupont, James K. McCarthy, Jared T. Broddrick, Miroslav Oborník, Aleš Horák, Zoltán Füssy, Jaromír Cihlář, Sabrina Kleessen, Hong Zheng, John P. McCrow, Kim K. Hixson, Wagner L. Araújo, Adriano Nunes-Nesi, Alisdair Fernie, Zoran Nikoloski, Bernhard O. Palsson and Andrew E. Allen ()
Additional contact information
Sarah R. Smith: J. Craig Venter Institute
Chris L. Dupont: J. Craig Venter Institute
James K. McCarthy: J. Craig Venter Institute
Jared T. Broddrick: University of California, San Diego
Miroslav Oborník: Biology Centre Czech Academy of Sciences
Aleš Horák: Biology Centre Czech Academy of Sciences
Zoltán Füssy: Biology Centre Czech Academy of Sciences
Jaromír Cihlář: Biology Centre Czech Academy of Sciences
Sabrina Kleessen: Targenomix, GmbH
Hong Zheng: J. Craig Venter Institute
John P. McCrow: J. Craig Venter Institute
Kim K. Hixson: Pacific Northwest National Laboratory
Wagner L. Araújo: Universidade Federal de Viçosa
Adriano Nunes-Nesi: Universidade Federal de Viçosa
Alisdair Fernie: Max Planck Institut of Molecular Plant Physiology
Zoran Nikoloski: University of Potsdam
Bernhard O. Palsson: University of California, San Diego
Andrew E. Allen: J. Craig Venter Institute

Nature Communications, 2019, vol. 10, issue 1, 1-14

Abstract: Abstract Diatoms outcompete other phytoplankton for nitrate, yet little is known about the mechanisms underpinning this ability. Genomes and genome-enabled studies have shown that diatoms possess unique features of nitrogen metabolism however, the implications for nutrient utilization and growth are poorly understood. Using a combination of transcriptomics, proteomics, metabolomics, fluxomics, and flux balance analysis to examine short-term shifts in nitrogen utilization in the model pennate diatom in Phaeodactylum tricornutum, we obtained a systems-level understanding of assimilation and intracellular distribution of nitrogen. Chloroplasts and mitochondria are energetically integrated at the critical intersection of carbon and nitrogen metabolism in diatoms. Pathways involved in this integration are organelle-localized GS-GOGAT cycles, aspartate and alanine systems for amino moiety exchange, and a split-organelle arginine biosynthesis pathway that clarifies the role of the diatom urea cycle. This unique configuration allows diatoms to efficiently adjust to changing nitrogen status, conferring an ecological advantage over other phytoplankton taxa.

Date: 2019
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DOI: 10.1038/s41467-019-12407-y

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