Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros

International audience Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms a...

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Published in:PLOS Biology
Main Authors: Nef, Charlotte, Madoui, Mohammed-Amin, Pelletier, Éric, Bowler, Chris
Other Authors: Génomique métabolique (UMR 8030), Genoscope - Centre national de séquençage Evry (GENOSCOPE), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS), Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE), Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN), Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili, Institut de biologie de l'ENS Paris (IBENS), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS-PSL), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2022
Subjects:
Online Access:https://cea.hal.science/cea-04321570
https://doi.org/10.1371/journal.pbio.3001893
id ftunivtoulon:oai:HAL:cea-04321570v1
record_format openpolar
institution Open Polar
collection Université de Toulon: HAL
op_collection_id ftunivtoulon
language English
topic [SDV]Life Sciences [q-bio]
spellingShingle [SDV]Life Sciences [q-bio]
Nef, Charlotte
Madoui, Mohammed-Amin
Pelletier, Éric
Bowler, Chris
Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
topic_facet [SDV]Life Sciences [q-bio]
description International audience Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros , the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data.
author2 Génomique métabolique (UMR 8030)
Genoscope - Centre national de séquençage Evry (GENOSCOPE)
Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA))
Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS)
Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE)
Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN)
Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili
Institut de biologie de l'ENS Paris (IBENS)
Département de Biologie - ENS Paris
École normale supérieure - Paris (ENS-PSL)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)
format Article in Journal/Newspaper
author Nef, Charlotte
Madoui, Mohammed-Amin
Pelletier, Éric
Bowler, Chris
author_facet Nef, Charlotte
Madoui, Mohammed-Amin
Pelletier, Éric
Bowler, Chris
author_sort Nef, Charlotte
title Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
title_short Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
title_full Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
title_fullStr Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
title_full_unstemmed Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros
title_sort whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom chaetoceros
publisher HAL CCSD
publishDate 2022
url https://cea.hal.science/cea-04321570
https://doi.org/10.1371/journal.pbio.3001893
genre Arctic
Arctic Ocean
Climate change
genre_facet Arctic
Arctic Ocean
Climate change
op_source ISSN: 1544-9173
EISSN: 1545-7885
PLoS Biology
https://cea.hal.science/cea-04321570
PLoS Biology, 2022, 20 (11), pp.e3001893. ⟨10.1371/journal.pbio.3001893⟩
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doi:10.1371/journal.pbio.3001893
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container_title PLOS Biology
container_volume 20
container_issue 11
container_start_page e3001893
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spelling ftunivtoulon:oai:HAL:cea-04321570v1 2024-05-19T07:35:26+00:00 Whole-genome scanning reveals environmental selection mechanisms that shape diversity in populations of the epipelagic diatom Chaetoceros Nef, Charlotte Madoui, Mohammed-Amin Pelletier, Éric Bowler, Chris Génomique métabolique (UMR 8030) Genoscope - Centre national de séquençage Evry (GENOSCOPE) Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)) Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Centre National de la Recherche Scientifique (CNRS) Global Oceans Systems Ecology & Evolution - Tara Oceans (GOSEE) Université de Perpignan Via Domitia (UPVD)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Aix Marseille Université (AMU)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université d'Évry-Val-d'Essonne (UEVE)-Université de Toulon (UTLN)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes 2016-2019 (UGA 2016-2019 )-Institut de Recherche pour le Développement (IRD France-Nord )-Ecole Normale Supérieure Paris-Saclay (ENS Paris Saclay)-European Molecular Biology Laboratory (EMBL)-NANTES UNIVERSITÉ - École Centrale de Nantes (Nantes Univ - ECN) Nantes Université (Nantes Univ)-Nantes Université (Nantes Univ)-Université australe du Chili Institut de biologie de l'ENS Paris (IBENS) Département de Biologie - ENS Paris École normale supérieure - Paris (ENS-PSL) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS-PSL) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) 2022-11-28 https://cea.hal.science/cea-04321570 https://doi.org/10.1371/journal.pbio.3001893 en eng HAL CCSD Public Library of Science info:eu-repo/semantics/altIdentifier/doi/10.1371/journal.pbio.3001893 cea-04321570 https://cea.hal.science/cea-04321570 doi:10.1371/journal.pbio.3001893 ISSN: 1544-9173 EISSN: 1545-7885 PLoS Biology https://cea.hal.science/cea-04321570 PLoS Biology, 2022, 20 (11), pp.e3001893. ⟨10.1371/journal.pbio.3001893⟩ [SDV]Life Sciences [q-bio] info:eu-repo/semantics/article Journal articles 2022 ftunivtoulon https://doi.org/10.1371/journal.pbio.3001893 2024-04-24T23:52:41Z International audience Diatoms form a diverse and abundant group of photosynthetic protists that are essential players in marine ecosystems. However, the microevolutionary structure of their populations remains poorly understood, particularly in polar regions. Exploring how closely related diatoms adapt to different environments is essential given their short generation times, which may allow rapid adaptations, and their prevalence in marine regions dramatically impacted by climate change, such as the Arctic and Southern Oceans. Here, we address genetic diversity patterns in Chaetoceros , the most abundant diatom genus and one of the most diverse, using 11 metagenome-assembled genomes (MAGs) reconstructed from Tara Oceans metagenomes. Genome-resolved metagenomics on these MAGs confirmed a prevalent distribution of Chaetoceros in the Arctic Ocean with lower dispersal in the Pacific and Southern Oceans as well as in the Mediterranean Sea. Single-nucleotide variants identified within the different MAG populations allowed us to draw a landscape of Chaetoceros genetic diversity and revealed an elevated genetic structure in some Arctic Ocean populations. Gene flow patterns of closely related Chaetoceros populations seemed to correlate with distinct abiotic factors rather than with geographic distance. We found clear positive selection of genes involved in nutrient availability responses, in particular for iron (e.g., ISIP2a, flavodoxin), silicate, and phosphate (e.g., polyamine synthase), that were further supported by analysis of Chaetoceros transcriptomes. Altogether, these results highlight the importance of environmental selection in shaping diatom diversity patterns and provide new insights into their metapopulation genomics through the integration of metagenomic and environmental data. Article in Journal/Newspaper Arctic Arctic Ocean Climate change Université de Toulon: HAL PLOS Biology 20 11 e3001893