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, Andrew E. Allen*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

20 Citations (Scopus)

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.

Original languageEnglish
Article number4552
JournalNature Communications
Volume10
Issue number1
DOIs
Publication statusPublished - 1 Dec 2019

Bibliographical note

Funding Information:
This study was supported by the National Science Foundation (NSF-MCB-1024913 and NSF-MCB-1818390) (to A.E.A.), the United States Department of Energy Genomics Science Program (DE-SC00006719 and DE-SC0008593 to A.E.A. and C.L.D. and DESC0008701 to B.O.P.), the Gordon and Betty Moore Foundation grant GBMF3828 (to A.E.A.), the Czech Science Foundation project 15-17643S and ERDF/ESF No.CZ.02.1.01/ 0.0/0.0/16_019/0000759 (to M.O.). A portion of the research was performed using EMSL, a national scientific user facility sponsored by the Department of Energy’s Office of Biological and Environmental Research and located at Pacific Northwest National Laboratory. Computational resources for construction of phylogenies were provided by MetaCentrum and CERIT-SC, Brno, Czech Republic.

Publisher Copyright:
© 2019, The Author(s).

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