Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO 2 Levels
Abstract
Diatoms are eukaryotic microalgae that are responsible for up to 40% of the ocean’s primary productivity. How diatoms respond to environmental perturbations such as elevated carbon concentrations in the atmosphere is currently poorly understood. We developed a transcriptional regulatory network based on various transcriptome sequencing expression libraries for different environmental responses to gain insight into the marine diatom’s metabolic and regulatory interactions and provide a comprehensive framework of responses to increasing atmospheric carbon levels. This transcriptional regulatory network was integrated with a recently published genome-scale metabolic model of Phaeodactylum tricornutum to explore the connectivity of the regulatory network and shared metabolites. The integrated regulatory and metabolic model revealed highly connected modules within carbon and nitrogen metabolism. P. tricornutum’s response to rising carbon levels was analyzed by using the recent genome-scale metabolic model with cross comparison to experimental manipulations of carbon dioxide. Using a systems biology approach, we studied the response of the marine diatom Phaeodactylum tricornutum to changing atmospheric carbon concentrations on an ocean-wide scale. By integrating an available genome-scale metabolic model and a newly developed transcriptional regulatory network inferred from transcriptome sequencing expression data, we demonstrate that carbon metabolism and nitrogen metabolism are strongly connected and the genes involvedmore »
- Authors:
-
- Department of Bioengineering, University of California San Diego, La Jolla, California, USA
- Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, California, USA
- Microbial and Environmental Genomics, J. Craig Venter Institute, La Jolla, California, USA, Integrative Oceanography Division, Scripps Institute of Oceanography, University of California San Diego, La Jolla, California, USA
- Publication Date:
- Research Org.:
- J. Craig Venter Inst., La Jolla, CA (United States); Univ. of California, San Diego, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF); Gordon and Betty Moore Foundation (United States)
- OSTI Identifier:
- 1618373
- Alternate Identifier(s):
- OSTI ID: 1423796
- Grant/Contract Number:
- DOE-DE-SC0008593; DOE-DE-SC0006719; SC0008593; SC0006719; MCB-1024913; MCB-1129303; GBMF3828
- Resource Type:
- Published Article
- Journal Name:
- mSystems
- Additional Journal Information:
- Journal Name: mSystems Journal Volume: 2 Journal Issue: 1; Journal ID: ISSN 2379-5077
- Publisher:
- American Society for Microbiology
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Phaeodactylum tricornutum; coregulated genes; genome-scale metabolic network reconstruction; integrated network modeling; regulatory network inference
Citation Formats
Levering, Jennifer, Dupont, Christopher L., Allen, Andrew E., Palsson, Bernhard O., Zengler, Karsten, and Lin, ed., Xiaoxia. Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO 2 Levels. United States: N. p., 2017.
Web. doi:10.1128/mSystems.00142-16.
Levering, Jennifer, Dupont, Christopher L., Allen, Andrew E., Palsson, Bernhard O., Zengler, Karsten, & Lin, ed., Xiaoxia. Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO 2 Levels. United States. https://doi.org/10.1128/mSystems.00142-16
Levering, Jennifer, Dupont, Christopher L., Allen, Andrew E., Palsson, Bernhard O., Zengler, Karsten, and Lin, ed., Xiaoxia. Tue .
"Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO 2 Levels". United States. https://doi.org/10.1128/mSystems.00142-16.
@article{osti_1618373,
title = {Integrated Regulatory and Metabolic Networks of the Marine Diatom Phaeodactylum tricornutum Predict the Response to Rising CO 2 Levels},
author = {Levering, Jennifer and Dupont, Christopher L. and Allen, Andrew E. and Palsson, Bernhard O. and Zengler, Karsten and Lin, ed., Xiaoxia},
abstractNote = {Diatoms are eukaryotic microalgae that are responsible for up to 40% of the ocean’s primary productivity. How diatoms respond to environmental perturbations such as elevated carbon concentrations in the atmosphere is currently poorly understood. We developed a transcriptional regulatory network based on various transcriptome sequencing expression libraries for different environmental responses to gain insight into the marine diatom’s metabolic and regulatory interactions and provide a comprehensive framework of responses to increasing atmospheric carbon levels. This transcriptional regulatory network was integrated with a recently published genome-scale metabolic model of Phaeodactylum tricornutum to explore the connectivity of the regulatory network and shared metabolites. The integrated regulatory and metabolic model revealed highly connected modules within carbon and nitrogen metabolism. P. tricornutum’s response to rising carbon levels was analyzed by using the recent genome-scale metabolic model with cross comparison to experimental manipulations of carbon dioxide. Using a systems biology approach, we studied the response of the marine diatom Phaeodactylum tricornutum to changing atmospheric carbon concentrations on an ocean-wide scale. By integrating an available genome-scale metabolic model and a newly developed transcriptional regulatory network inferred from transcriptome sequencing expression data, we demonstrate that carbon metabolism and nitrogen metabolism are strongly connected and the genes involved are coregulated in this model diatom. These tight regulatory constraints could play a major role during the adaptation of P. tricornutum to increasing carbon levels. The transcriptional regulatory network developed can be further used to study the effects of different environmental perturbations on P. tricornutum’s metabolism.},
doi = {10.1128/mSystems.00142-16},
journal = {mSystems},
number = 1,
volume = 2,
place = {United States},
year = {Tue Feb 28 00:00:00 EST 2017},
month = {Tue Feb 28 00:00:00 EST 2017}
}
https://doi.org/10.1128/mSystems.00142-16
Web of Science
Works referenced in this record:
Recent advances in reconstruction and applications of genome-scale metabolic models
journal, August 2012
- Kim, Tae Yong; Sohn, Seung Bum; Kim, Yu Bin
- Current Opinion in Biotechnology, Vol. 23, Issue 4
Inactivation of Phaeodactylum tricornutum urease gene using transcription activator-like effector nuclease-based targeted mutagenesis
journal, October 2014
- Weyman, Philip D.; Beeri, Karen; Lefebvre, Stephane C.
- Plant Biotechnology Journal, Vol. 13, Issue 4
Chloroplast genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana: comparison with other plastid genomes of the red lineage
journal, January 2007
- Oudot-Le Secq, Marie-Pierre; Grimwood, Jane; Shapiro, Harris
- Molecular Genetics and Genomics, Vol. 277, Issue 4
optGpSampler: An Improved Tool for Uniformly Sampling the Solution-Space of Genome-Scale Metabolic Networks
journal, February 2014
- Megchelenbrink, Wout; Huynen, Martijn; Marchiori, Elena
- PLoS ONE, Vol. 9, Issue 2
Comparative analysis of diatom genomes reveals substantial differences in the organization of carbon partitioning pathways
journal, May 2012
- Smith, Sarah R.; Abbriano, Raffaela M.; Hildebrand, Mark
- Algal Research, Vol. 1, Issue 1
STRING v10: protein–protein interaction networks, integrated over the tree of life
journal, October 2014
- Szklarczyk, Damian; Franceschini, Andrea; Wyder, Stefan
- Nucleic Acids Research, Vol. 43, Issue D1
Complex repeat structures and novel features in the mitochondrial genomes of the diatoms Phaeodactylum tricornutum and Thalassiosira pseudonana
journal, May 2011
- Secq, Marie-Pierre Oudot-Le; Green, Beverley R.
- Gene, Vol. 476, Issue 1-2
Transcription factor families inferred from genome sequences of photosynthetic stramenopiles
journal, July 2010
- Rayko, Edda; Maumus, Florian; Maheswari, Uma
- New Phytologist, Vol. 188, Issue 1
Quantitative prediction of cellular metabolism with constraint-based models: the COBRA Toolbox v2.0
journal, August 2011
- Schellenberger, Jan; Que, Richard; Fleming, Ronan M. T.
- Nature Protocols, Vol. 6, Issue 9
Oceanographic and Biogeochemical Insights from Diatom Genomes
journal, January 2010
- Bowler, Chris; Vardi, Assaf; Allen, Andrew E.
- Annual Review of Marine Science, Vol. 2, Issue 1
Adjusting batch effects in microarray expression data using empirical Bayes methods
journal, April 2006
- Johnson, W. Evan; Li, Cheng; Rabinovic, Ariel
- Biostatistics, Vol. 8, Issue 1
cMonkey 2 : Automated, systematic, integrated detection of co-regulated gene modules for any organism
journal, April 2015
- Reiss, David J.; Plaisier, Christopher L.; Wu, Wei-Ju
- Nucleic Acids Research, Vol. 43, Issue 13
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
limma powers differential expression analyses for RNA-sequencing and microarray studies
journal, January 2015
- Ritchie, Matthew E.; Phipson, Belinda; Wu, Di
- Nucleic Acids Research, Vol. 43, Issue 7
What is flux balance analysis?
journal, March 2010
- Orth, Jeffrey D.; Thiele, Ines; Palsson, Bernhard Ø
- Nature Biotechnology, Vol. 28, Issue 3
Anthropogenic carbon and ocean pH
journal, September 2003
- Caldeira, Ken; Wickett, Michael E.
- Nature, Vol. 425, Issue 6956
The physiology and genetics of CO2 concentrating mechanisms in model diatoms
journal, June 2016
- Hopkinson, Brian M.; Dupont, Christopher L.; Matsuda, Yusuke
- Current Opinion in Plant Biology, Vol. 31
Differential expression analysis for sequence count data
journal, October 2010
- Anders, Simon; Huber, Wolfgang
- Genome Biology, Vol. 11, Issue 10
Production and dissolution of biogenic silica in the ocean: Revised global estimates, comparison with regional data and relationship to biogenic sedimentation
journal, September 1995
- Nelson, David M.; Tréguer, Paul; Brzezinski, Mark A.
- Global Biogeochemical Cycles, Vol. 9, Issue 3
Genome-Scale Model Reveals Metabolic Basis of Biomass Partitioning in a Model Diatom
journal, May 2016
- Levering, Jennifer; Broddrick, Jared; Dupont, Christopher L.
- PLOS ONE, Vol. 11, Issue 5
Constraining the metabolic genotype–phenotype relationship using a phylogeny of in silico methods
journal, February 2012
- Lewis, Nathan E.; Nagarajan, Harish; Palsson, Bernhard O.
- Nature Reviews Microbiology, Vol. 10, Issue 4