Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome

Abstract Deciphering how microbial communities are shaped by environmental variability is fundamental for understanding the structure and function of ocean ecosystems. While seasonal environmental gradients have been shown to structure the taxonomic dynamics of microbiomes over time, little is known...

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Main Authors: Taylor Priest, Ellen Oldenburg, Ovidiu Popa, Bledina Dede, Katja Metfies, Wilken-Jon von Appen, Sinhué Torres-Valdés, Christina Bienhold, Bernhard M. Fuchs, Rudolf Amann, Antje Boetius, Matthias Wietz
Format: Article
Language:English
Published: Nature Portfolio 2025-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-56203-3
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author Taylor Priest
Ellen Oldenburg
Ovidiu Popa
Bledina Dede
Katja Metfies
Wilken-Jon von Appen
Sinhué Torres-Valdés
Christina Bienhold
Bernhard M. Fuchs
Rudolf Amann
Antje Boetius
Matthias Wietz
author_facet Taylor Priest
Ellen Oldenburg
Ovidiu Popa
Bledina Dede
Katja Metfies
Wilken-Jon von Appen
Sinhué Torres-Valdés
Christina Bienhold
Bernhard M. Fuchs
Rudolf Amann
Antje Boetius
Matthias Wietz
author_sort Taylor Priest
collection DOAJ
description Abstract Deciphering how microbial communities are shaped by environmental variability is fundamental for understanding the structure and function of ocean ecosystems. While seasonal environmental gradients have been shown to structure the taxonomic dynamics of microbiomes over time, little is known about their impact on functional dynamics and the coupling between taxonomy and function. Here, we demonstrate annually recurrent, seasonal structuring of taxonomic and functional dynamics in a pelagic Arctic Ocean microbiome by combining autonomous samplers and in situ sensors with long-read metagenomics and SSU ribosomal metabarcoding. Specifically, we identified five temporal microbiome modules whose succession within each annual cycle represents a transition across different ecological states. For instance, Cand. Nitrosopumilus, Syndiniales, and the machinery to oxidise ammonia and reduce nitrite are signatures of early polar night, while late summer is characterised by Amylibacter and sulfur compound metabolism. Leveraging metatranscriptomes from Tara Oceans, we also demonstrate the consistency in functional dynamics across the wider Arctic Ocean during similar temporal periods. Furthermore, the structuring of genetic diversity within functions over time indicates that environmental selection pressure acts heterogeneously on microbiomes across seasons. By integrating taxonomic, functional and environmental information, our study provides fundamental insights into how microbiomes are structured under pronounced seasonal changes in understudied, yet rapidly changing polar marine ecosystems.
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spelling doaj-art-bdeb342bd1744fb7b87bca632fcd5a732025-02-09T12:44:39ZengNature PortfolioNature Communications2041-17232025-02-0116111310.1038/s41467-025-56203-3Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiomeTaylor Priest0Ellen Oldenburg1Ovidiu Popa2Bledina Dede3Katja Metfies4Wilken-Jon von Appen5Sinhué Torres-Valdés6Christina Bienhold7Bernhard M. Fuchs8Rudolf Amann9Antje Boetius10Matthias Wietz11Max Planck Institute for Marine MicrobiologyInstitute for Quantitative and Theoretical Biology, Heinrich Heine University DüsseldorfInstitute for Quantitative and Theoretical Biology, Heinrich Heine University DüsseldorfMax Planck Institute for Marine MicrobiologyAlfred Wegener Institute Helmholtz Centre for Polar and Marine ResearchAlfred Wegener Institute Helmholtz Centre for Polar and Marine ResearchAlfred Wegener Institute Helmholtz Centre for Polar and Marine ResearchMax Planck Institute for Marine MicrobiologyMax Planck Institute for Marine MicrobiologyMax Planck Institute for Marine MicrobiologyMax Planck Institute for Marine MicrobiologyMax Planck Institute for Marine MicrobiologyAbstract Deciphering how microbial communities are shaped by environmental variability is fundamental for understanding the structure and function of ocean ecosystems. While seasonal environmental gradients have been shown to structure the taxonomic dynamics of microbiomes over time, little is known about their impact on functional dynamics and the coupling between taxonomy and function. Here, we demonstrate annually recurrent, seasonal structuring of taxonomic and functional dynamics in a pelagic Arctic Ocean microbiome by combining autonomous samplers and in situ sensors with long-read metagenomics and SSU ribosomal metabarcoding. Specifically, we identified five temporal microbiome modules whose succession within each annual cycle represents a transition across different ecological states. For instance, Cand. Nitrosopumilus, Syndiniales, and the machinery to oxidise ammonia and reduce nitrite are signatures of early polar night, while late summer is characterised by Amylibacter and sulfur compound metabolism. Leveraging metatranscriptomes from Tara Oceans, we also demonstrate the consistency in functional dynamics across the wider Arctic Ocean during similar temporal periods. Furthermore, the structuring of genetic diversity within functions over time indicates that environmental selection pressure acts heterogeneously on microbiomes across seasons. By integrating taxonomic, functional and environmental information, our study provides fundamental insights into how microbiomes are structured under pronounced seasonal changes in understudied, yet rapidly changing polar marine ecosystems.https://doi.org/10.1038/s41467-025-56203-3
spellingShingle Taylor Priest
Ellen Oldenburg
Ovidiu Popa
Bledina Dede
Katja Metfies
Wilken-Jon von Appen
Sinhué Torres-Valdés
Christina Bienhold
Bernhard M. Fuchs
Rudolf Amann
Antje Boetius
Matthias Wietz
Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
Nature Communications
title Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
title_full Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
title_fullStr Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
title_full_unstemmed Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
title_short Seasonal recurrence and modular assembly of an Arctic pelagic marine microbiome
title_sort seasonal recurrence and modular assembly of an arctic pelagic marine microbiome
url https://doi.org/10.1038/s41467-025-56203-3
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