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

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 insigh...

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Autores principales: Lavoie, Michel, Saint-Béat, Blanche, Strauss, Jan, Guérin, Sébastien, Allard, Antoine, V. Hardy, Simon, Falciatore, Angela, Lavaud, Johann
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168318/
https://www.ncbi.nlm.nih.gov/pubmed/32079178
http://dx.doi.org/10.3390/biology9020030
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author Lavoie, Michel
Saint-Béat, Blanche
Strauss, Jan
Guérin, Sébastien
Allard, Antoine
V. Hardy, Simon
Falciatore, Angela
Lavaud, Johann
author_facet Lavoie, Michel
Saint-Béat, Blanche
Strauss, Jan
Guérin, Sébastien
Allard, Antoine
V. Hardy, Simon
Falciatore, Angela
Lavaud, Johann
author_sort Lavoie, Michel
collection PubMed
description 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.
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spelling pubmed-71683182020-04-22 Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness Lavoie, Michel Saint-Béat, Blanche Strauss, Jan Guérin, Sébastien Allard, Antoine V. Hardy, Simon Falciatore, Angela Lavaud, Johann Biology (Basel) Article 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. MDPI 2020-02-17 /pmc/articles/PMC7168318/ /pubmed/32079178 http://dx.doi.org/10.3390/biology9020030 Text en © 2020 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Lavoie, Michel
Saint-Béat, Blanche
Strauss, Jan
Guérin, Sébastien
Allard, Antoine
V. Hardy, Simon
Falciatore, Angela
Lavaud, Johann
Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title_full Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title_fullStr Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title_full_unstemmed Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title_short Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
title_sort genome-scale metabolic reconstruction and in silico perturbation analysis of the polar diatom fragilariopsis cylindrus predicts high metabolic robustness
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7168318/
https://www.ncbi.nlm.nih.gov/pubmed/32079178
http://dx.doi.org/10.3390/biology9020030
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