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

Abstract

Diatoms dominate phytoplankton communities by outcompeting other taxa for nitrogen, yet little is known about the molecular underpinnings of this ability. As a consequence of their evolutionary history, diatoms possess traits that are both autotroph- and heterotroph-like expanding their metabolic capabilities beyond other model organisms. Here we use the model marine diatom Phaeodactylum tricornutum to investigate the extent to which diatoms have combined elements of nitrogen metabolism from each ancestral partner. Using a range of experimental and metabolic modeling approaches, we found compartment-specific assimilation of different forms of nitrogen, requiring the operation of metabolite shuttles to synchronize organellar metabolism. Further we identified a hybrid arginine biosynthesis pathway, clarifying the role of the urea cycle in diatoms. We conclude that metabolic integration between the major energy organelles, established post-endosymbiosis in diatoms, confers an advantage for nitrogen utilization of and contributes to their ecological success in a highly dynamic marine environment.

Authors:
 [1];  [1]; ORCiD logo [1];  [2];  [3];  [3]; ORCiD logo [3];  [3];  [4];  [1];  [1]; ORCiD logo [5]; ORCiD logo [6];  [7];  [8];  [9]; ORCiD logo [10]; ORCiD logo [11]
+ Show Author Affiliations
  1. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics
  2. Univ. of California, San Diego, La Jolla, CA (United States). Div. of Biological Sciences and Dept. of Bioengineering
  3. Biology Centre Czech Academy of Sciences, České Budějovice (Czech Republic). Inst. of Parasitology; Univ. of South Bohemia, České Budějovice (Czech Republic). Faculty of Science
  4. Targenomix, GmbH, Potsdam (Germany)
  5. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab.
  6. Univ. Federal de Vicosa, Minas Gerais (Brazil). Dept. de Biologia Vegetal and Max-Planck Partner Group at the Dept. de Biologia Vegetal
  7. Univ. Federal de Vicosa, Minas Gerais (Brazil). Dept. de Biologia Vegetal
  8. Max Planck Inst. of Molecular Plant Physiology, Potsdam (Germany)
  9. Univ. of Potsdam, Potsdam (Germany). Inst. of Biochemistry and Biology
  10. Univ. of California, San Diego, La Jolla, CA (United States). Dept. of Bioengineering
  11. J. Craig Venter Inst., La Jolla, CA (United States). Microbial and Environmental Genomics; Univ. of California, San Diego, La Jolla, CA (United States). Scripps Inst. of Oceanography, Integrative Oceanography Div.
Publication Date:
Research Org.:
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE
OSTI Identifier:
1577080
Report Number(s):
PNNL-SA-137295
Journal ID: ISSN 2041-1723
Grant/Contract Number:  
AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature Communications
Additional Journal Information:
Journal Volume: 10; Journal Issue: 1; Journal ID: ISSN 2041-1723
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; diatom; nitrogen; flux balance analysis; transcriptomics; proteomics

Citation Formats

Smith, Sarah R., Dupont, Chris L., McCarthy, James K., Broddrick, Jared T., Oborník, Miroslav, Horák, Aleš, Füssy, Zoltán, Cihlář, Jaromír, Kleessen, Sabrina, Zheng, Hong, McCrow, John P., Hixson, Kim K., Araújo, Wagner L., Nunes-Nesi, Adriano, Fernie, Alisdair, Nikoloski, Zoran, Palsson, Bernhard O., and Allen, Andrew E. Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom. United States: N. p., 2019. Web. doi:10.1038/s41467-019-12407-y.
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Smith, Sarah R., Dupont, Chris L., McCarthy, James K., Broddrick, Jared T., Oborník, Miroslav, Horák, Aleš, Füssy, Zoltán, Cihlář, Jaromír, Kleessen, Sabrina, Zheng, Hong, McCrow, John P., Hixson, Kim K., Araújo, Wagner L., Nunes-Nesi, Adriano, Fernie, Alisdair, Nikoloski, Zoran, Palsson, Bernhard O., & Allen, Andrew E. Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom. United States. doi:10.1038/s41467-019-12407-y.
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Smith, Sarah R., Dupont, Chris L., McCarthy, James K., Broddrick, Jared T., Oborník, Miroslav, Horák, Aleš, Füssy, Zoltán, Cihlář, Jaromír, Kleessen, Sabrina, Zheng, Hong, McCrow, John P., Hixson, Kim K., Araújo, Wagner L., Nunes-Nesi, Adriano, Fernie, Alisdair, Nikoloski, Zoran, Palsson, Bernhard O., and Allen, Andrew E. Mon . "Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom". United States. doi:10.1038/s41467-019-12407-y. https://www.osti.gov/servlets/purl/1577080.
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@article{osti_1577080,
title = {Evolution and regulation of nitrogen flux through compartmentalized metabolic networks in a marine diatom},
author = {Smith, Sarah R. and Dupont, Chris L. and McCarthy, James K. and Broddrick, Jared T. and Oborník, Miroslav and Horák, Aleš and Füssy, Zoltán and Cihlář, Jaromír and Kleessen, Sabrina and Zheng, Hong and McCrow, John P. and Hixson, Kim K. and Araújo, Wagner L. and Nunes-Nesi, Adriano and Fernie, Alisdair and Nikoloski, Zoran and Palsson, Bernhard O. and Allen, Andrew E.},
abstractNote = {Diatoms dominate phytoplankton communities by outcompeting other taxa for nitrogen, yet little is known about the molecular underpinnings of this ability. As a consequence of their evolutionary history, diatoms possess traits that are both autotroph- and heterotroph-like expanding their metabolic capabilities beyond other model organisms. Here we use the model marine diatom Phaeodactylum tricornutum to investigate the extent to which diatoms have combined elements of nitrogen metabolism from each ancestral partner. Using a range of experimental and metabolic modeling approaches, we found compartment-specific assimilation of different forms of nitrogen, requiring the operation of metabolite shuttles to synchronize organellar metabolism. Further we identified a hybrid arginine biosynthesis pathway, clarifying the role of the urea cycle in diatoms. We conclude that metabolic integration between the major energy organelles, established post-endosymbiosis in diatoms, confers an advantage for nitrogen utilization of and contributes to their ecological success in a highly dynamic marine environment.},
doi = {10.1038/s41467-019-12407-y},
journal = {Nature Communications},
number = 1,
volume = 10,
place = {United States},
year = {2019},
month = {10}
}
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DOI:  10.1038/s41467-019-12407-y
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