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

SR. Smith, CL. Dupont, JK. McCarthy, JT. Broddrick, M. Oborník, A. Horák, Z. Füssy, J. Cihlář, S. Kleessen, H. Zheng, JP. McCrow, KK. Hixson, WL. Araújo, A. Nunes-Nesi, A. Fernie, Z. Nikoloski, BO. Palsson, AE. Allen,

. 2019 ; 10 (1) : 4552. [pub] 20191007

Language English Country Great Britain

Document type Journal Article, Research Support, Non-U.S. Gov't, Research Support, U.S. Gov't, Non-P.H.S.

Persistent link   https://www.medvik.cz/link/bmc20005820

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.

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$a Diatoms outcompete other phytoplankton for nitrate, yet little is known about the mechanisms underpinning this ability. Genomes and genome-enabled studies have shown that diatoms possess unique features of nitrogen metabolism however, the implications for nutrient utilization and growth are poorly understood. Using a combination of transcriptomics, proteomics, metabolomics, fluxomics, and flux balance analysis to examine short-term shifts in nitrogen utilization in the model pennate diatom in Phaeodactylum tricornutum, we obtained a systems-level understanding of assimilation and intracellular distribution of nitrogen. Chloroplasts and mitochondria are energetically integrated at the critical intersection of carbon and nitrogen metabolism in diatoms. Pathways involved in this integration are organelle-localized GS-GOGAT cycles, aspartate and alanine systems for amino moiety exchange, and a split-organelle arginine biosynthesis pathway that clarifies the role of the diatom urea cycle. This unique configuration allows diatoms to efficiently adjust to changing nitrogen status, conferring an ecological advantage over other phytoplankton taxa.
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$a Dupont, Chris L $u Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.
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$a McCarthy, James K $u Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.
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$a Broddrick, Jared T $u Division of Biological Sciences, University of California, San Diego, La Jolla, CA, 92093, USA. Department of Bioengineering, University of California, San Diego, La Jolla, CA, 92093, USA.
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$a Oborník, Miroslav $u Institute of Parasitology, Biology Centre Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic.
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$a Horák, Aleš $u Institute of Parasitology, Biology Centre Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic.
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$a Füssy, Zoltán $u Institute of Parasitology, Biology Centre Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic.
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$a Cihlář, Jaromír $u Institute of Parasitology, Biology Centre Czech Academy of Sciences, Branišovská 31, 370 05, České Budějovice, Czech Republic. Faculty of Science, University of South Bohemia, Branišovská 31, 370 05, České Budějovice, Czech Republic.
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$a Kleessen, Sabrina $u Targenomix, GmbH, Wissenschaftspark Potsdam-Golm, 14476, Potsdam, Germany.
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$a Zheng, Hong $u Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.
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$a McCrow, John P $u Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA.
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$a Hixson, Kim K $u Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland, WA, 99352, USA.
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$a Araújo, Wagner L $u Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil. Max-Planck Partner Group at the Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil.
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$a Nunes-Nesi, Adriano $u Departamento de Biologia Vegetal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, 36570-900, Brazil.
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$a Fernie, Alisdair $u Max Planck Institut of Molecular Plant Physiology, Am Mühlenberg 1, 14476, Potsdam, Germany.
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$a Nikoloski, Zoran $u Institute of Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, 14476, Potsdam, Germany.
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$a Palsson, Bernhard O $u Department of Bioengineering, University of California, San Diego, La Jolla, CA, 92093, USA.
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$a Allen, Andrew E $u Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, CA, 92037, USA. aallen@jcvi.org. Scripps Institution of Oceanography, Integrative Oceanography Division, University of California, San Diego, La Jolla, CA, 92093, USA. aallen@jcvi.org.
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