skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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]
  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.
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.
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.
@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}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Save / Share:

Works referenced in this record:

Profiling of the Early Nitrogen Stress Response in the Diatom Phaeodactylum tricornutum Reveals a Novel Family of RING-Domain Transcription Factors
journal, November 2015

  • Matthijs, Michiel; Fabris, Michele; Broos, Stefan
  • Plant Physiology, Vol. 170, Issue 1
  • DOI: 10.1104/pp.15.01300

Proteomics to reveal metabolic network shifts towards lipid accumulation following nitrogen deprivation in the diatom Phaeodactylum tricornutum
journal, May 2013


MitoFates: Improved Prediction of Mitochondrial Targeting Sequences and Their Cleavage Sites
journal, February 2015

  • Fukasawa, Yoshinori; Tsuji, Junko; Fu, Szu-Chin
  • Molecular & Cellular Proteomics, Vol. 14, Issue 4
  • DOI: 10.1074/mcp.M114.043083

The Genome of the Diatom Thalassiosira Pseudonana: Ecology, Evolution, and Metabolism
journal, October 2004


The PRIDE database and related tools and resources in 2019: improving support for quantification data
journal, November 2018

  • Perez-Riverol, Yasset; Csordas, Attila; Bai, Jingwen
  • Nucleic Acids Research, Vol. 47, Issue D1
  • DOI: 10.1093/nar/gky1106

Nitrate Reductase Knockout Uncouples Nitrate Transport from Nitrate Assimilation and Drives Repartitioning of Carbon Flux in a Model Pennate Diatom
journal, August 2017

  • McCarthy, James K.; Smith, Sarah R.; McCrow, John P.
  • The Plant Cell, Vol. 29, Issue 8
  • DOI: 10.1105/tpc.16.00910

HECTAR: A method to predict subcellular targeting in heterokonts
journal, January 2008

  • Gschloessl, Bernhard; Guermeur, Yann; Cock, J. Mark
  • BMC Bioinformatics, Vol. 9, Issue 1
  • DOI: 10.1186/1471-2105-9-393

Ammonium inhibition of nitrate uptake by the diatom, Phaeodactylum tricornutum
journal, April 1979


Locating proteins in the cell using TargetP, SignalP and related tools
journal, April 2007

  • Emanuelsson, Olof; Brunak, Søren; von Heijne, Gunnar
  • Nature Protocols, Vol. 2, Issue 4
  • DOI: 10.1038/nprot.2007.131

C hlamydomonas  NZF1, a tandem-repeated zinc finger factor involved in nitrate signalling by controlling the regulatory gene NIT 2 : Nitrate signalling in
journal, March 2014

  • Higuera, Jose Javier; Fernandez, Emilio; Galvan, Aurora
  • Plant, Cell & Environment, Vol. 37, Issue 9
  • DOI: 10.1111/pce.12305

Whole-cell response to nitrogen deprivation in the diatom Phaeodactylum tricornutum
journal, July 2015

  • Alipanah, Leila; Rohloff, Jens; Winge, Per
  • Journal of Experimental Botany, Vol. 66, Issue 20
  • DOI: 10.1093/jxb/erv340

The Generating Function of CID, ETD, and CID/ETD Pairs of Tandem Mass Spectra: Applications to Database Search
journal, September 2010

  • Kim, Sangtae; Mischerikow, Nikolai; Bandeira, Nuno
  • Molecular & Cellular Proteomics, Vol. 9, Issue 12
  • DOI: 10.1074/mcp.M110.003731

Gas chromatography mass spectrometry–based metabolite profiling in plants
journal, June 2006

  • Lisec, Jan; Schauer, Nicolas; Kopka, Joachim
  • Nature Protocols, Vol. 1, Issue 1
  • DOI: 10.1038/nprot.2006.59

The Phaeodactylum genome reveals the evolutionary history of diatom genomes
journal, October 2008

  • Bowler, Chris; Allen, Andrew E.; Badger, Jonathan H.
  • Nature, Vol. 456, Issue 7219
  • DOI: 10.1038/nature07410

Plastid proteome prediction for diatoms and other algae with secondary plastids of the red lineage
journal, January 2015

  • Gruber, Ansgar; Rocap, Gabrielle; Kroth, Peter G.
  • The Plant Journal, Vol. 81, Issue 3
  • DOI: 10.1111/tpj.12734

Global analysis of protein expression in yeast
journal, October 2003

  • Ghaemmaghami, Sina; Huh, Won-Ki; Bower, Kiowa
  • Nature, Vol. 425, Issue 6959
  • DOI: 10.1038/nature02046

Comparison of laboratory and in situ measurements of urea decomposition by a marine diatom
journal, May 1972

  • Carpenter, Edward J.; Remsen, Charles C.; Schroeder, Brian W.
  • Journal of Experimental Marine Biology and Ecology, Vol. 8, Issue 3
  • DOI: 10.1016/0022-0981(72)90065-2

Transcription factor evolution in eukaryotes and the assembly of the regulatory toolkit in multicellular lineages
journal, November 2013

  • de Mendoza, A.; Sebe-Pedros, A.; Sestak, M. S.
  • Proceedings of the National Academy of Sciences, Vol. 110, Issue 50
  • DOI: 10.1073/pnas.1311818110

Genes, enzymes and regulation of arginine biosynthesis in plants
journal, August 2005


An NMRA-Like Protein Regulates Gene Expression in Phytophthora capsici to Drive the Infection Cycle on Tomato
journal, June 2018

  • Pham, Jasmine; Stam, Remco; Heredia, Victor Martinez
  • Molecular Plant-Microbe Interactions, Vol. 31, Issue 6
  • DOI: 10.1094/MPMI-07-17-0193-R

Chemically Etched Open Tubular and Monolithic Emitters for Nanoelectrospray Ionization Mass Spectrometry
journal, November 2006

  • Kelly, Ryan T.; Page, Jason S.; Luo, Quanzhou
  • Analytical Chemistry, Vol. 78, Issue 22, p. 7796-7801
  • DOI: 10.1021/ac061133r

An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database
journal, November 1994

  • Eng, Jimmy K.; McCormack, Ashley L.; Yates, John R.
  • Journal of the American Society for Mass Spectrometry, Vol. 5, Issue 11
  • DOI: 10.1016/1044-0305(94)80016-2

Computational Method to Predict Mitochondrially Imported Proteins and their Targeting Sequences
journal, November 1996


Evolution and metabolic significance of the urea cycle in photosynthetic diatoms
journal, May 2011

  • Allen, Andrew E.; Dupont, Christopher L.; Oborník, Miroslav
  • Nature, Vol. 473, Issue 7346
  • DOI: 10.1038/nature10074

A Diatom Gene Regulating Nitric-Oxide Signaling and Susceptibility to Diatom-Derived Aldehydes
journal, June 2008


MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability
journal, January 2013

  • Katoh, K.; Standley, D. M.
  • Molecular Biology and Evolution, Vol. 30, Issue 4
  • DOI: 10.1093/molbev/mst010

Plant nitrogen assimilation and its regulation: a complex puzzle with missing pieces
journal, June 2015


Nuclear retention of the transcription factor NLP7 orchestrates the early response to nitrate in plants
journal, April 2013

  • Marchive, Chloé; Roudier, François; Castaings, Loren
  • Nature Communications, Vol. 4, Issue 1
  • DOI: 10.1038/ncomms2650

IQ-TREE: A Fast and Effective Stochastic Algorithm for Estimating Maximum-Likelihood Phylogenies
journal, November 2014

  • Nguyen, Lam-Tung; Schmidt, Heiko A.; von Haeseler, Arndt
  • Molecular Biology and Evolution, Vol. 32, Issue 1
  • DOI: 10.1093/molbev/msu300

AtNOS/AtNOA1 Is a Functional Arabidopsis thaliana cGTPase and Not a Nitric-oxide Synthase
journal, September 2008

  • Moreau, Magali; Lee, Gyu In; Wang, Yongzeng
  • Journal of Biological Chemistry, Vol. 283, Issue 47
  • DOI: 10.1074/jbc.M804838200

MASIC: A software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC–MS(/MS) features
journal, June 2008


THB1, a truncated hemoglobin, modulates nitric oxide levels and nitrate reductase activity
journal, January 2015

  • Sanz-Luque, Emanuel; Ocaña-Calahorro, Francisco; de Montaigu, Amaury
  • The Plant Journal, Vol. 81, Issue 3
  • DOI: 10.1111/tpj.12744

GC-MS libraries for the rapid identification of metabolites in complex biological samples
journal, January 2005


Genome-Scale Model Reveals Metabolic Basis of Biomass Partitioning in a Model Diatom
journal, May 2016


The role of functional traits and trade-offs in structuring phytoplankton communities: scaling from cellular to ecosystem level
journal, December 2007


COBRApy: COnstraints-Based Reconstruction and Analysis for Python
journal, January 2013

  • Ebrahim, Ali; Lerman, Joshua A.; Palsson, Bernhard O.
  • BMC Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1186/1752-0509-7-74

Orchestration of transcriptome, proteome and metabolome in the diatom Phaeodactylum tricornutum during nitrogen limitation
journal, November 2018


NtcA, a global nitrogen regulator from the cyanobacterium Synechococcus that belongs to the Crp family of bacterial regulators
journal, July 1992


The place of diatoms in the biofuels industry
journal, March 2012

  • Hildebrand, Mark; Davis, Aubrey K.; Smith, Sarah R.
  • Biofuels, Vol. 3, Issue 2
  • DOI: 10.4155/bfs.11.157

R2R3-type MYB transcription factor, CmMYB1, is a central nitrogen assimilation regulator in Cyanidioschyzon merolae
journal, July 2009

  • Imamura, S.; Kanesaki, Y.; Ohnuma, M.
  • Proceedings of the National Academy of Sciences, Vol. 106, Issue 30
  • DOI: 10.1073/pnas.0902790106

Cross‐compartment metabolic coupling enables flexible photoprotective mechanisms in the diatom Phaeodactylum tricornutum
journal, February 2019

  • Broddrick, Jared T.; Du, Niu; Smith, Sarah R.
  • New Phytologist, Vol. 222, Issue 3
  • DOI: 10.1111/nph.15685

ModelFinder: fast model selection for accurate phylogenetic estimates
journal, May 2017

  • Kalyaanamoorthy, Subha; Minh, Bui Quang; Wong, Thomas K. F.
  • Nature Methods, Vol. 14, Issue 6
  • DOI: 10.1038/nmeth.4285

edgeR: a Bioconductor package for differential expression analysis of digital gene expression data
journal, November 2009


Energetic coupling between plastids and mitochondria drives CO2 assimilation in diatoms
journal, July 2015

  • Bailleul, Benjamin; Berne, Nicolas; Murik, Omer
  • Nature, Vol. 524, Issue 7565
  • DOI: 10.1038/nature14599

Transformation of Nonselectable Reporter Genes in Marine Diatoms
journal, May 1999

  • Falciatore, Angela; Casotti, Raffaella; Leblanc, Catherine
  • Marine Biotechnology, Vol. 1, Issue 3
  • DOI: 10.1007/PL00011773

Phytoplankton succession and nitrogen utilization during the development of an upwelling bloom
journal, May 2011

  • Fawcett, Se; Ward, Bb
  • Marine Ecology Progress Series, Vol. 428
  • DOI: 10.3354/meps09070

The Mixed Lineage Nature of Nitrogen Transport and Assimilation in Marine Eukaryotic Phytoplankton: A Case Study of Micromonas
journal, May 2010

  • McDonald, Sarah M.; Plant, Joshua N.; Worden, Alexandra Z.
  • Molecular Biology and Evolution, Vol. 27, Issue 10
  • DOI: 10.1093/molbev/msq113

trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses
journal, June 2009


Whole-cell response of the pennate diatom Phaeodactylum tricornutum to iron starvation
journal, July 2008

  • Allen, A. E.; LaRoche, J.; Maheswari, U.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 30
  • DOI: 10.1073/pnas.0711370105

Flux profiling of photosynthetic carbon metabolism in intact plants
journal, July 2014

  • Heise, Robert; Arrivault, Stéphanie; Szecowka, Marek
  • Nature Protocols, Vol. 9, Issue 8
  • DOI: 10.1038/nprot.2014.115

Remodeling of intermediate metabolism in the diatom Phaeodactylum tricornutum under nitrogen stress
journal, December 2014

  • Levitan, Orly; Dinamarca, Jorge; Zelzion, Ehud
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 2
  • DOI: 10.1073/pnas.1419818112

Comparative evaluation of certain organic and inorganic sources of nitrogen for phototrophic growth of marine microalgae
journal, August 1975

  • Antia, N. J.; Berland, B. R.; Bonin, D. J.
  • Journal of the Marine Biological Association of the United Kingdom, Vol. 55, Issue 3
  • DOI: 10.1017/S0025315400017239

Recommendations for Reporting Metabolite Data
journal, July 2011

  • Fernie, Alisdair R.; Aharoni, Asaph; Willmitzer, Lothar
  • The Plant Cell, Vol. 23, Issue 7
  • DOI: 10.1105/tpc.111.086272

BLAST+: architecture and applications
journal, January 2009

  • Camacho, Christiam; Coulouris, George; Avagyan, Vahram
  • BMC Bioinformatics, Vol. 10, Issue 1
  • DOI: 10.1186/1471-2105-10-421

Uptake of Nitrate by the Diatom Phaeodactylum tricornutum
journal, January 1981

  • Cresswell, R. C.; Syrett, P. J.
  • Journal of Experimental Botany, Vol. 32, Issue 1
  • DOI: 10.1093/jxb/32.1.19

Analysis of raphidophyte assimilatory nitrate reductase reveals unique domain architecture incorporating a 2/2 hemoglobin
journal, October 2011


Quantifying similarity between motifs
journal, January 2007

  • Gupta, Shobhit; Stamatoyannopoulos, John A.; Bailey, Timothy L.
  • Genome Biology, Vol. 8, Issue 2
  • DOI: 10.1186/gb-2007-8-2-r24

JASPAR 2018: update of the open-access database of transcription factor binding profiles and its web framework
journal, November 2017

  • Khan, Aziz; Fornes, Oriol; Stigliani, Arnaud
  • Nucleic Acids Research, Vol. 46, Issue D1
  • DOI: 10.1093/nar/gkx1126

Elucidating dynamic metabolic physiology through network integration of quantitative time-course metabolomics
journal, April 2017

  • Bordbar, Aarash; Yurkovich, James T.; Paglia, Giuseppe
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep46249

Chloroplast-mitochondria cross-talk in diatoms
journal, January 2012

  • Prihoda, J.; Tanaka, A.; de Paula, W. B. M.
  • Journal of Experimental Botany, Vol. 63, Issue 4
  • DOI: 10.1093/jxb/err441

Transcription factor families inferred from genome sequences of photosynthetic stramenopiles
journal, July 2010


PII in higher plants: a modern role for an ancient protein
journal, September 2009


Growth of marine planktonic diatoms on inorganic and organic nitrogen
journal, January 1982


Integration of transcriptomics and metabolomics data specifies the metabolic response of Chlamydomonas to rapamycin treatment
journal, February 2015

  • Kleessen, Sabrina; Irgang, Susann; Klie, Sebastian
  • The Plant Journal, Vol. 81, Issue 5
  • DOI: 10.1111/tpj.12763

Understanding nitrate assimilation and its regulation in microalgae
journal, October 2015

  • Sanz-Luque, Emanuel; Chamizo-Ampudia, Alejandro; Llamas, Angel
  • Frontiers in Plant Science, Vol. 6
  • DOI: 10.3389/fpls.2015.00899

Transcriptional Orchestration of the Global Cellular Response of a Model Pennate Diatom to Diel Light Cycling under Iron Limitation
journal, December 2016


A novel protein, Pho92, has a conserved YTH domain and regulates phosphate metabolism by decreasing the mRNA stability of PHO4 in Saccharomyces cerevisiae
journal, January 2014

  • Kang, Hyun-Jun; Jeong, Sook-Jin; Kim, Kyung-Nam
  • Biochemical Journal, Vol. 457, Issue 3
  • DOI: 10.1042/BJ20130862

Phosphorylation by MPK6: A conserved transcriptional modification mediates nitrate reductase activation and NO production?
journal, June 2011

  • Wang, Pengcheng; Du, Yanyan; Song, Chun-Peng
  • Plant Signaling & Behavior, Vol. 6, Issue 6
  • DOI: 10.4161/psb.6.6.15308

Reversed-phase chromatography with multiple fraction concatenation strategy for proteome profiling of human MCF10A cells
journal, April 2011


Molecular toolbox for studying diatom biology in Phaeodactylum tricornutum
journal, December 2007