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Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies

The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by...

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Autores principales: Doré, Hugo, Guyet, Ulysse, Leconte, Jade, Farrant, Gregory K., Alric, Benjamin, Ratin, Morgane, Ostrowski, Martin, Ferrieux, Mathilde, Brillet-Guéguen, Loraine, Hoebeke, Mark, Siltanen, Jukka, Le Corguillé, Gildas, Corre, Erwan, Wincker, Patrick, Scanlan, David J., Eveillard, Damien, Partensky, Frédéric, Garczarek, Laurence
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10119275/
https://www.ncbi.nlm.nih.gov/pubmed/36841901
http://dx.doi.org/10.1038/s41396-023-01386-0
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author Doré, Hugo
Guyet, Ulysse
Leconte, Jade
Farrant, Gregory K.
Alric, Benjamin
Ratin, Morgane
Ostrowski, Martin
Ferrieux, Mathilde
Brillet-Guéguen, Loraine
Hoebeke, Mark
Siltanen, Jukka
Le Corguillé, Gildas
Corre, Erwan
Wincker, Patrick
Scanlan, David J.
Eveillard, Damien
Partensky, Frédéric
Garczarek, Laurence
author_facet Doré, Hugo
Guyet, Ulysse
Leconte, Jade
Farrant, Gregory K.
Alric, Benjamin
Ratin, Morgane
Ostrowski, Martin
Ferrieux, Mathilde
Brillet-Guéguen, Loraine
Hoebeke, Mark
Siltanen, Jukka
Le Corguillé, Gildas
Corre, Erwan
Wincker, Patrick
Scanlan, David J.
Eveillard, Damien
Partensky, Frédéric
Garczarek, Laurence
author_sort Doré, Hugo
collection PubMed
description The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change.
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spelling pubmed-101192752023-04-22 Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies Doré, Hugo Guyet, Ulysse Leconte, Jade Farrant, Gregory K. Alric, Benjamin Ratin, Morgane Ostrowski, Martin Ferrieux, Mathilde Brillet-Guéguen, Loraine Hoebeke, Mark Siltanen, Jukka Le Corguillé, Gildas Corre, Erwan Wincker, Patrick Scanlan, David J. Eveillard, Damien Partensky, Frédéric Garczarek, Laurence ISME J Article The ever-increasing number of available microbial genomes and metagenomes provides new opportunities to investigate the links between niche partitioning and genome evolution in the ocean, especially for the abundant and ubiquitous marine picocyanobacteria Prochlorococcus and Synechococcus. Here, by combining metagenome analyses of the Tara Oceans dataset with comparative genomics, including phyletic patterns and genomic context of individual genes from 256 reference genomes, we show that picocyanobacterial communities thriving in different niches possess distinct gene repertoires. We also identify clusters of adjacent genes that display specific distribution patterns in the field (eCAGs) and are thus potentially involved in the same metabolic pathway and may have a key role in niche adaptation. Several eCAGs are likely involved in the uptake or incorporation of complex organic forms of nutrients, such as guanidine, cyanate, cyanide, pyrimidine, or phosphonates, which might be either directly used by cells, for example for the biosynthesis of proteins or DNA, or degraded to inorganic nitrogen and/or phosphorus forms. We also highlight the enrichment of eCAGs involved in polysaccharide capsule biosynthesis in Synechococcus populations thriving in both nitrogen- and phosphorus-depleted areas vs. low-iron (Fe) regions, suggesting that the complexes they encode may be too energy-consuming for picocyanobacteria thriving in the latter areas. In contrast, Prochlorococcus populations thriving in Fe-depleted areas specifically possess an alternative respiratory terminal oxidase, potentially involved in the reduction of Fe(III) to Fe(II). Altogether, this study provides insights into how phytoplankton communities populate oceanic ecosystems, which is relevant to understanding their capacity to respond to ongoing climate change. Nature Publishing Group UK 2023-02-25 2023-05 /pmc/articles/PMC10119275/ /pubmed/36841901 http://dx.doi.org/10.1038/s41396-023-01386-0 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Doré, Hugo
Guyet, Ulysse
Leconte, Jade
Farrant, Gregory K.
Alric, Benjamin
Ratin, Morgane
Ostrowski, Martin
Ferrieux, Mathilde
Brillet-Guéguen, Loraine
Hoebeke, Mark
Siltanen, Jukka
Le Corguillé, Gildas
Corre, Erwan
Wincker, Patrick
Scanlan, David J.
Eveillard, Damien
Partensky, Frédéric
Garczarek, Laurence
Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title_full Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title_fullStr Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title_full_unstemmed Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title_short Differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
title_sort differential global distribution of marine picocyanobacteria gene clusters reveals distinct niche-related adaptive strategies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10119275/
https://www.ncbi.nlm.nih.gov/pubmed/36841901
http://dx.doi.org/10.1038/s41396-023-01386-0
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