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Open AccessArticle

Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness

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Unité Mixte Internationale 3376 Takuvik, CNRS-ULaval, Département de Biologie and Québec-Océan, Université Laval, Québec, QC G1V 0A6, Canada
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Department of Biology, University of Hamburg, D-22607 Hamburg, Germany
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CSSB Centre for Structural Systems Biology, c/o Deutsches Elektronen-Synchrotron DESY, Notkestraße 85, D-22607 Hamburg, Germany
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Département de physique, de génie physique et d’optique, Université Laval, Québec, QC G1V 0A6, Canada
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Centre interdisciplinaire de modélisation mathématique, Université Laval, Québec, QC G1V 0A6, Canada
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Département d’informatique et génie logiciel, Département de biochimie, microbiologie et bio-informatique, Université Laval, Québec, QC G1V 0A6, Canada
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Unité des Neurosciences cellulaires et moléculaires, Centre de recherche CERVO, Québec, QC G1V 0A6, Canada
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Institut de Biologie Physico-Chimique, Laboratory of Chloroplast Biology and Light Sensing in Microalgae, UMR7141, Centre National de la Recherche Scientifique (CNRS), Sorbonne Université, 75005 Paris, France
*
Author to whom correspondence should be addressed.
Biology 2020, 9(2), 30; https://doi.org/10.3390/biology9020030
Received: 15 December 2019 / Revised: 31 January 2020 / Accepted: 8 February 2020 / Published: 17 February 2020
(This article belongs to the Special Issue The Molecular Life of Diatoms: From Genes to Ecosystems)
Diatoms are major primary producers in polar environments where they can actively grow under extremely variable conditions. Integrative modeling using a genome-scale model (GSM) is a powerful approach to decipher the complex interactions between components of diatom metabolism and can provide insights into metabolic mechanisms underlying their evolutionary success in polar ecosystems. We developed the first GSM for a polar diatom, Fragilariopsis cylindrus, which enabled us to study its metabolic robustness using sensitivity analysis. We find that the predicted growth rate was robust to changes in all model parameters (i.e., cell biochemical composition) except the carbon uptake rate. Constraints on total cellular carbon buffer the effect of changes in the input parameters on reaction fluxes and growth rate. We also show that single reaction deletion of 20% to 32% of active (nonzero flux) reactions and single gene deletion of 44% to 55% of genes associated with active reactions affected the growth rate, as well as the production fluxes of total protein, lipid, carbohydrate, DNA, RNA, and pigments by less than 1%, which was due to the activation of compensatory reactions (e.g., analogous enzymes and alternative pathways) with more highly connected metabolites involved in the reactions that were robust to deletion. Interestingly, including highly divergent alleles unique for F. cylindrus increased its metabolic robustness to cellular perturbations even more. Overall, our results underscore the high robustness of metabolism in F. cylindrus, a feature that likely helps to maintain cell homeostasis under polar conditions. View Full-Text
Keywords: flux balance analysis; metabolic network; arctic; systems biology; reaction deletion; gene deletion flux balance analysis; metabolic network; arctic; systems biology; reaction deletion; gene deletion
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MDPI and ACS Style

Lavoie, M.; Saint-Béat, B.; Strauss, J.; Guérin, S.; Allard, A.; V. Hardy, S.; Falciatore, A.; Lavaud, J. Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness. Biology 2020, 9, 30. https://doi.org/10.3390/biology9020030

AMA Style

Lavoie M, Saint-Béat B, Strauss J, Guérin S, Allard A, V. Hardy S, Falciatore A, Lavaud J. Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness. Biology. 2020; 9(2):30. https://doi.org/10.3390/biology9020030

Chicago/Turabian Style

Lavoie, Michel; Saint-Béat, Blanche; Strauss, Jan; Guérin, Sébastien; Allard, Antoine; V. Hardy, Simon; Falciatore, Angela; Lavaud, Johann. 2020. "Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness" Biology 9, no. 2: 30. https://doi.org/10.3390/biology9020030

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