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

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 envir...

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Published in:PLOS Biology
Main Authors: Nef, Charlotte, Madoui, Mohammed-Amin, Pelletier, Éric, Bowler, Chris
Other Authors: Eloe-Fadrosh, Emiley, HORIZON EUROPE European Research Council, Agence Nationale de la Recherche, Université de Recherche Paris Sciences et Lettres
Format: Article in Journal/Newspaper
Language:English
Published: Public Library of Science (PLoS) 2022
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Online Access:http://dx.doi.org/10.1371/journal.pbio.3001893
https://dx.plos.org/10.1371/journal.pbio.3001893
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spelling crplos:10.1371/journal.pbio.3001893 2024-09-30T14:30:13+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 Eloe-Fadrosh, Emiley HORIZON EUROPE European Research Council HORIZON EUROPE European Research Council Agence Nationale de la Recherche Université de Recherche Paris Sciences et Lettres Agence Nationale de la Recherche Agence Nationale de la Recherche 2022 http://dx.doi.org/10.1371/journal.pbio.3001893 https://dx.plos.org/10.1371/journal.pbio.3001893 en eng Public Library of Science (PLoS) http://creativecommons.org/licenses/by/4.0/ PLOS Biology volume 20, issue 11, page e3001893 ISSN 1545-7885 journal-article 2022 crplos https://doi.org/10.1371/journal.pbio.3001893 2024-09-10T04:17:28Z 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 PLOS Arctic Arctic Ocean Pacific PLOS Biology 20 11 e3001893
institution Open Polar
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op_collection_id crplos
language English
description 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 Eloe-Fadrosh, Emiley
HORIZON EUROPE European Research Council
HORIZON EUROPE European Research Council
Agence Nationale de la Recherche
Université de Recherche Paris Sciences et Lettres
Agence Nationale de la Recherche
Agence Nationale de la Recherche
format Article in Journal/Newspaper
author Nef, Charlotte
Madoui, Mohammed-Amin
Pelletier, Éric
Bowler, Chris
spellingShingle 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
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 Public Library of Science (PLoS)
publishDate 2022
url http://dx.doi.org/10.1371/journal.pbio.3001893
https://dx.plos.org/10.1371/journal.pbio.3001893
geographic Arctic
Arctic Ocean
Pacific
geographic_facet Arctic
Arctic Ocean
Pacific
genre Arctic
Arctic Ocean
Climate change
genre_facet Arctic
Arctic Ocean
Climate change
op_source PLOS Biology
volume 20, issue 11, page e3001893
ISSN 1545-7885
op_rights http://creativecommons.org/licenses/by/4.0/
op_doi https://doi.org/10.1371/journal.pbio.3001893
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