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.

Departamento de Biologia Vegetal Universidade Federal de Viçosa Viçosa Minas Gerais 36570 900 Brazil

Department of Bioengineering University of California San Diego La Jolla CA 92093 USA

Division of Biological Sciences University of California San Diego La Jolla CA 92093 USA

Environmental Molecular Sciences Laboratory Pacific Northwest National Laboratory Richland WA 99352 USA

Faculty of Science University of South Bohemia Branišovská 31 370 05 České Budějovice Czech Republic

Institute of Biochemistry and Biology University of Potsdam Karl Liebknecht Str 24 25 14476 Potsdam Germany

Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 31 370 05 České Budějovice Czech Republic

Max Planck Institut of Molecular Plant Physiology Am Mühlenberg 1 14476 Potsdam Germany

Max Planck Partner Group at the Departamento de Biologia Vegetal Universidade Federal de Viçosa Viçosa Minas Gerais 36570 900 Brazil

Microbial and Environmental Genomics J Craig Venter Institute La Jolla CA 92037 USA

Scripps Institution of Oceanography Integrative Oceanography Division University of California San Diego La Jolla CA 92093 USA

Targenomix GmbH Wissenschaftspark Potsdam Golm 14476 Potsdam Germany

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