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

Authors
  • Lavoie, Michel1
  • Saint-Béat, Blanche1
  • Strauss, Jan2
  • Guérin, Sébastien1
  • Allard, Antoine3
  • V. Hardy, Simon4
  • Falciatore, Angela
  • Lavaud, Johann1
  • 1 (J.L.)
  • 2 CSSB Centre for Structural Systems Biology, c/o Deutsches Elektronen-Synchrotron DESY, Notkestraße 85, D-22607 Hamburg, Germany
  • 3 Centre interdisciplinaire de modélisation mathématique, Université Laval, Québec, QC G1V 0A6, Canada
  • 4 Unité des Neurosciences cellulaires et moléculaires, Centre de recherche CERVO, Québec, QC G1V 0A6, Canada
Type
Published Article
Journal
Biology
Publisher
MDPI
Publication Date
Feb 17, 2020
Volume
9
Issue
2
Identifiers
DOI: 10.3390/biology9020030
PMID: 32079178
PMCID: PMC7168318
Source
PubMed Central
Keywords
License
Green

Abstract

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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