Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness
International audience 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...
Published in: | Biology |
---|---|
Main Authors: | , , , , , , , |
Other Authors: | , , , , , , |
Format: | Article in Journal/Newspaper |
Language: | English |
Published: |
HAL CCSD
2020
|
Subjects: | |
Online Access: | https://hal.science/hal-02481799 https://hal.science/hal-02481799/document https://hal.science/hal-02481799/file/2020b-Biology.pdf https://doi.org/10.3390/biology9020030 |
id |
ftsorbonneuniv:oai:HAL:hal-02481799v1 |
---|---|
record_format |
openpolar |
spelling |
ftsorbonneuniv:oai:HAL:hal-02481799v1 2024-05-12T08:00:28+00:00 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 Guerin, Sébastien Allard, Antoine Hardy, Simon, V Falciatore, Angela Lavaud, Johann Takuvik Joint International Laboratory ULAVAL-CNRS Université Laval Québec (ULaval)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS) Universität Hamburg (UHH) Université Laval Québec (ULaval) Biologie du chloroplaste et perception de la lumière chez les micro-algues Institut de biologie physico-chimique (IBPC (FR_550)) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) 2020 https://hal.science/hal-02481799 https://hal.science/hal-02481799/document https://hal.science/hal-02481799/file/2020b-Biology.pdf https://doi.org/10.3390/biology9020030 en eng HAL CCSD MDPI info:eu-repo/semantics/altIdentifier/doi/10.3390/biology9020030 hal-02481799 https://hal.science/hal-02481799 https://hal.science/hal-02481799/document https://hal.science/hal-02481799/file/2020b-Biology.pdf doi:10.3390/biology9020030 info:eu-repo/semantics/OpenAccess ISSN: 2079-7737 Biology https://hal.science/hal-02481799 Biology, 2020, 9, pp.30. ⟨10.3390/biology9020030⟩ flux balance analysis metabolic network arctic systems biology reaction deletion gene deletion [SDV.BV]Life Sciences [q-bio]/Vegetal Biology [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology info:eu-repo/semantics/article Journal articles 2020 ftsorbonneuniv https://doi.org/10.3390/biology9020030 2024-04-18T03:42:06Z International audience 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. Article in Journal/Newspaper Arctic HAL Sorbonne Université Arctic Biology 9 2 30 |
institution |
Open Polar |
collection |
HAL Sorbonne Université |
op_collection_id |
ftsorbonneuniv |
language |
English |
topic |
flux balance analysis metabolic network arctic systems biology reaction deletion gene deletion [SDV.BV]Life Sciences [q-bio]/Vegetal Biology [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology |
spellingShingle |
flux balance analysis metabolic network arctic systems biology reaction deletion gene deletion [SDV.BV]Life Sciences [q-bio]/Vegetal Biology [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology Lavoie, Michel Saint-Béat, Blanche Strauss, Jan Guerin, Sébastien Allard, Antoine Hardy, Simon, V Falciatore, Angela Lavaud, Johann Genome-Scale Metabolic Reconstruction and in Silico Perturbation Analysis of the Polar Diatom Fragilariopsis cylindrus Predicts High Metabolic Robustness |
topic_facet |
flux balance analysis metabolic network arctic systems biology reaction deletion gene deletion [SDV.BV]Life Sciences [q-bio]/Vegetal Biology [SDV.MP]Life Sciences [q-bio]/Microbiology and Parasitology |
description |
International audience 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. |
author2 |
Takuvik Joint International Laboratory ULAVAL-CNRS Université Laval Québec (ULaval)-Institut national des sciences de l'Univers (INSU - CNRS)-Centre National de la Recherche Scientifique (CNRS) Universität Hamburg (UHH) Université Laval Québec (ULaval) Biologie du chloroplaste et perception de la lumière chez les micro-algues Institut de biologie physico-chimique (IBPC (FR_550)) Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS) |
format |
Article in Journal/Newspaper |
author |
Lavoie, Michel Saint-Béat, Blanche Strauss, Jan Guerin, Sébastien Allard, Antoine Hardy, Simon, V Falciatore, Angela Lavaud, Johann |
author_facet |
Lavoie, Michel Saint-Béat, Blanche Strauss, Jan Guerin, Sébastien Allard, Antoine Hardy, Simon, V Falciatore, Angela Lavaud, Johann |
author_sort |
Lavoie, Michel |
title |
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_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_sort |
genome-scale metabolic reconstruction and in silico perturbation analysis of the polar diatom fragilariopsis cylindrus predicts high metabolic robustness |
publisher |
HAL CCSD |
publishDate |
2020 |
url |
https://hal.science/hal-02481799 https://hal.science/hal-02481799/document https://hal.science/hal-02481799/file/2020b-Biology.pdf https://doi.org/10.3390/biology9020030 |
geographic |
Arctic |
geographic_facet |
Arctic |
genre |
Arctic |
genre_facet |
Arctic |
op_source |
ISSN: 2079-7737 Biology https://hal.science/hal-02481799 Biology, 2020, 9, pp.30. ⟨10.3390/biology9020030⟩ |
op_relation |
info:eu-repo/semantics/altIdentifier/doi/10.3390/biology9020030 hal-02481799 https://hal.science/hal-02481799 https://hal.science/hal-02481799/document https://hal.science/hal-02481799/file/2020b-Biology.pdf doi:10.3390/biology9020030 |
op_rights |
info:eu-repo/semantics/OpenAccess |
op_doi |
https://doi.org/10.3390/biology9020030 |
container_title |
Biology |
container_volume |
9 |
container_issue |
2 |
container_start_page |
30 |
_version_ |
1798842354297208832 |