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Title: Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana

Abstract

Diatoms are one of the most productive and successful photosynthetic taxa on Earth and possess attributes such as rapid growth rates and production of lipids, making them candidate sources of renewable fuels. Despite their significance, few details of the mechanisms used to regulate growth and carbon metabolism are currently known, hindering metabolic engineering approaches to enhance productivity. To characterize the transcript level component of metabolic regulation, genome-wide changes in transcript abundance were documented in the model diatom Thalassiosira pseudonana on a time-course of silicon starvation. Growth, cell cycle progression, chloroplast replication, fatty acid composition, pigmentation, and photosynthetic parameters were characterized alongside lipid accumulation. Extensive coordination of large suites of genes was observed, highlighting the existence of clusters of coregulated genes as a key feature of global gene regulation in T. pseudonana. The identity of key enzymes for carbon metabolic pathway inputs (photosynthesis) and outputs (growth and storage) reveals these clusters are organized to synchronize these processes. Coordinated transcript level responses to silicon starvation are probably driven by signals linked to cell cycle progression and shifts in photophysiology. A mechanistic understanding of how this is accomplished will aid efforts to engineer metabolism for development of algal-derived biofuels.

Authors:
 [1];  [2];  [2];  [2];  [2];  [2];  [2];  [1];  [2]
  1. Univ. of California, San Diego, CA (United States). Scripps Institution of Oceanography; J. Craig Venter Inst. (JCVI), La Jolla, CA (United States)
  2. Univ. of California, San Diego, CA (United States). Scripps Institution of Oceanography
Publication Date:
Research Org.:
Univ. of California, San Diego, CA (United States); J. Craig Venter Inst. (JCVI), La Jolla, CA (United States)
Sponsoring Org.:
USDOE Office of Energy Efficiency and Renewable Energy (EERE), Sustainable Transportation Office. Bioenergy Technologies Office (BETO); USDOE Office of Science (SC), Biological and Environmental Research (BER); US Air Force Office of Scientific Research (AFOSR); National Science Foundation (NSF); California Energy Commission (United States); Gordon and Betty Moore Foundation (United States)
OSTI Identifier:
1437597
Grant/Contract Number:  
EE0001222; EE0003373; SC0006719; SC0008593; FA9550-08-1-0178; CBET-0903712; MCB-1024913; OCE-0727997; OCE-1140042; 500-10-039; GBMF3828
Resource Type:
Accepted Manuscript
Journal Name:
New Phytologist
Additional Journal Information:
Journal Volume: 210; Journal Issue: 3; Journal ID: ISSN 0028-646X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; carbon metabolism; cell cycle; diatom; lipid metabolism; Thalassiosira pseudonana; transcriptomics

Citation Formats

Smith, Sarah R., Gle, Corine, Abbriano, Raffaela M., Traller, Jesse C., Davis, Aubrey, Trentacoste, Emily, Vernet, Maria, Allen, Andrew E., and Hildebrand, Mark. Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana. United States: N. p., 2016. Web. doi:10.1111/nph.13843.
Smith, Sarah R., Gle, Corine, Abbriano, Raffaela M., Traller, Jesse C., Davis, Aubrey, Trentacoste, Emily, Vernet, Maria, Allen, Andrew E., & Hildebrand, Mark. Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana. United States. https://doi.org/10.1111/nph.13843
Smith, Sarah R., Gle, Corine, Abbriano, Raffaela M., Traller, Jesse C., Davis, Aubrey, Trentacoste, Emily, Vernet, Maria, Allen, Andrew E., and Hildebrand, Mark. Thu . "Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana". United States. https://doi.org/10.1111/nph.13843. https://www.osti.gov/servlets/purl/1437597.
@article{osti_1437597,
title = {Transcript level coordination of carbon pathways during silicon starvation-induced lipid accumulation in the diatom Thalassiosira pseudonana},
author = {Smith, Sarah R. and Gle, Corine and Abbriano, Raffaela M. and Traller, Jesse C. and Davis, Aubrey and Trentacoste, Emily and Vernet, Maria and Allen, Andrew E. and Hildebrand, Mark},
abstractNote = {Diatoms are one of the most productive and successful photosynthetic taxa on Earth and possess attributes such as rapid growth rates and production of lipids, making them candidate sources of renewable fuels. Despite their significance, few details of the mechanisms used to regulate growth and carbon metabolism are currently known, hindering metabolic engineering approaches to enhance productivity. To characterize the transcript level component of metabolic regulation, genome-wide changes in transcript abundance were documented in the model diatom Thalassiosira pseudonana on a time-course of silicon starvation. Growth, cell cycle progression, chloroplast replication, fatty acid composition, pigmentation, and photosynthetic parameters were characterized alongside lipid accumulation. Extensive coordination of large suites of genes was observed, highlighting the existence of clusters of coregulated genes as a key feature of global gene regulation in T. pseudonana. The identity of key enzymes for carbon metabolic pathway inputs (photosynthesis) and outputs (growth and storage) reveals these clusters are organized to synchronize these processes. Coordinated transcript level responses to silicon starvation are probably driven by signals linked to cell cycle progression and shifts in photophysiology. A mechanistic understanding of how this is accomplished will aid efforts to engineer metabolism for development of algal-derived biofuels.},
doi = {10.1111/nph.13843},
journal = {New Phytologist},
number = 3,
volume = 210,
place = {United States},
year = {Thu Feb 04 00:00:00 EST 2016},
month = {Thu Feb 04 00:00:00 EST 2016}
}

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Digital expression profiling of novel diatom transcripts provides insight into their biological functions
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Genome and low-iron response of an oceanic diatom adapted to chronic iron limitation
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TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions
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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
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Incorporating Motif Analysis into Gene Co-expression Networks Reveals Novel Modular Expression Pattern and New Signaling Pathways
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Choreography of the Transcriptome, Photophysiology, and Cell Cycle of a Minimal Photoautotroph, Prochlorococcus
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An Integrated Analysis of Molecular Acclimation to High Light in the Marine Diatom Phaeodactylum tricornutum
journal, November 2009


Aureochrome 1a Is Involved in the Photoacclimation of the Diatom Phaeodactylum tricornutum
journal, September 2013


Environmental control of plant nuclear gene expression by chloroplast redox signals
journal, January 2012

  • Pfalz, Jeannette; Liebers, Monique; Hirth, Matthias
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  • DOI: 10.1186/s13068-016-0670-3

Proteomic study uncovers molecular principles of single-cell-level phenotypic heterogeneity in lipid storage of Nannochloropsis oceanica
journal, February 2019


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


Meta-Omics Reveals Genetic Flexibility of Diatom Nitrogen Transporters in Response to Environmental Changes
journal, July 2019

  • Busseni, Greta; Rocha Jimenez Vieira, Fabio; Amato, Alberto
  • Molecular Biology and Evolution, Vol. 36, Issue 11
  • DOI: 10.1093/molbev/msz157

Regulation of the Calvin–Benson–Bassham cycle in the enigmatic diatoms: biochemical and evolutionary variations on an original theme
journal, July 2017

  • Jensen, Erik; Clément, Romain; Maberly, Stephen C.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
  • DOI: 10.1098/rstb.2016.0401

The effects of phosphorus limitation on carbon metabolism in diatoms
journal, July 2017

  • Brembu, Tore; Mühlroth, Alice; Alipanah, Leila
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
  • DOI: 10.1098/rstb.2016.0406

Structure and properties of oil bodies in diatoms
journal, July 2017

  • Maeda, Yoshiaki; Nojima, Daisuke; Yoshino, Tomoko
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
  • DOI: 10.1098/rstb.2016.0408

Reduced vacuolar β-1,3-glucan synthesis affects carbohydrate metabolism as well as plastid homeostasis and structure in Phaeodactylum tricornutum
journal, April 2018

  • Huang, Weichao; Haferkamp, Ilka; Lepetit, Bernard
  • Proceedings of the National Academy of Sciences, Vol. 115, Issue 18
  • DOI: 10.1073/pnas.1719274115

Expression of Histophilus somni IbpA DR2 protective antigen in the diatom Thalassiosira pseudonana
journal, April 2017

  • Davis, Aubrey; Crum, Lauren T.; Corbeil, Lynette B.
  • Applied Microbiology and Biotechnology, Vol. 101, Issue 13
  • DOI: 10.1007/s00253-017-8267-8

Meta-Omics Reveals Genetic Flexibility of Diatom Nitrogen Transporters in Response to Environmental Changes
journal, July 2019

  • Busseni, Greta; Rocha Jimenez Vieira, Fabio; Amato, Alberto
  • Molecular Biology and Evolution, Vol. 36, Issue 11
  • DOI: 10.1093/molbev/msz157

Regulation of the Calvin–Benson–Bassham cycle in the enigmatic diatoms: biochemical and evolutionary variations on an original theme
journal, July 2017

  • Jensen, Erik; Clément, Romain; Maberly, Stephen C.
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
  • DOI: 10.1098/rstb.2016.0401

The effects of phosphorus limitation on carbon metabolism in diatoms
journal, July 2017

  • Brembu, Tore; Mühlroth, Alice; Alipanah, Leila
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 372, Issue 1728
  • DOI: 10.1098/rstb.2016.0406

Genome and methylome of the oleaginous diatom Cyclotella cryptica reveal genetic flexibility toward a high lipid phenotype
journal, November 2016

  • Traller, Jesse C.; Cokus, Shawn J.; Lopez, David A.
  • Biotechnology for Biofuels, Vol. 9, Issue 1
  • DOI: 10.1186/s13068-016-0670-3

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


Improving ‘Lipid Productivity’ in Microalgae by Bilateral Enhancement of Biomass and Lipid Contents: A Review
journal, October 2020

  • Shokravi, Zahra; Shokravi, Hoofar; Chyuan, Ong Hwai
  • Sustainability, Vol. 12, Issue 21
  • DOI: 10.3390/su12219083