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Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community

Progress in molecular methods has enabled the monitoring of bacterial populations in time. Nevertheless, understanding community dynamics and its links with ecosystem functioning remains challenging due to the tremendous diversity of microorganisms. Conceptual frameworks that make sense of time seri...

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Autores principales: Massing, Jana C, Fahimipour, Ashkaan K., Bunse, Carina, Pinhassi, Jarone, Gross, Thilo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312292/
https://www.ncbi.nlm.nih.gov/pubmed/37255288
http://dx.doi.org/10.1128/msystems.00028-23
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author Massing, Jana C
Fahimipour, Ashkaan K.
Bunse, Carina
Pinhassi, Jarone
Gross, Thilo
author_facet Massing, Jana C
Fahimipour, Ashkaan K.
Bunse, Carina
Pinhassi, Jarone
Gross, Thilo
author_sort Massing, Jana C
collection PubMed
description Progress in molecular methods has enabled the monitoring of bacterial populations in time. Nevertheless, understanding community dynamics and its links with ecosystem functioning remains challenging due to the tremendous diversity of microorganisms. Conceptual frameworks that make sense of time series of taxonomically rich bacterial communities, regarding their potential ecological function, are needed. A key concept for organizing ecological functions is the niche, the set of strategies that enable a population to persist and define its impacts on the surroundings. Here we present a framework based on manifold learning to organize genomic information into potentially occupied bacterial metabolic niches over time. Manifold learning tries to uncover low-dimensional data structures in high-dimensional data sets that can be used to describe the data in reduced dimensions. We apply the method to re-construct the dynamics of putatively occupied metabolic niches using a long-term bacterial time series from the Baltic Sea, the Linnaeus Microbial Observatory (LMO). The results reveal a relatively low-dimensional space of occupied metabolic niches comprising groups of taxa with similar functional capabilities. Time patterns of occupied niches were strongly driven by seasonality. Some metabolic niches were dominated by one bacterial taxon, whereas others were occupied by multiple taxa, depending on the season. These results illustrate the power of manifold learning approaches to advance our understanding of the links between community composition and functioning in microbial systems. IMPORTANCE: The increase in data availability of bacterial communities highlights the need for conceptual frameworks to advance our understanding of these complex and diverse communities alongside the production of such data. To understand the dynamics of these tremendously diverse communities, we need tools to identify overarching strategies and describe their role and function in the ecosystem in a comprehensive way. Here, we show that a manifold learning approach can coarse grain bacterial communities in terms of their metabolic strategies and that we can thereby quantitatively organize genomic information in terms of potentially occupied niches over time. This approach, therefore, advances our understanding of how fluctuations in bacterial abundances and species composition can relate to ecosystem functions and it can facilitate the analysis, monitoring, and future predictions of the development of microbial communities.
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spelling pubmed-103122922023-07-01 Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community Massing, Jana C Fahimipour, Ashkaan K. Bunse, Carina Pinhassi, Jarone Gross, Thilo mSystems Research Article Progress in molecular methods has enabled the monitoring of bacterial populations in time. Nevertheless, understanding community dynamics and its links with ecosystem functioning remains challenging due to the tremendous diversity of microorganisms. Conceptual frameworks that make sense of time series of taxonomically rich bacterial communities, regarding their potential ecological function, are needed. A key concept for organizing ecological functions is the niche, the set of strategies that enable a population to persist and define its impacts on the surroundings. Here we present a framework based on manifold learning to organize genomic information into potentially occupied bacterial metabolic niches over time. Manifold learning tries to uncover low-dimensional data structures in high-dimensional data sets that can be used to describe the data in reduced dimensions. We apply the method to re-construct the dynamics of putatively occupied metabolic niches using a long-term bacterial time series from the Baltic Sea, the Linnaeus Microbial Observatory (LMO). The results reveal a relatively low-dimensional space of occupied metabolic niches comprising groups of taxa with similar functional capabilities. Time patterns of occupied niches were strongly driven by seasonality. Some metabolic niches were dominated by one bacterial taxon, whereas others were occupied by multiple taxa, depending on the season. These results illustrate the power of manifold learning approaches to advance our understanding of the links between community composition and functioning in microbial systems. IMPORTANCE: The increase in data availability of bacterial communities highlights the need for conceptual frameworks to advance our understanding of these complex and diverse communities alongside the production of such data. To understand the dynamics of these tremendously diverse communities, we need tools to identify overarching strategies and describe their role and function in the ecosystem in a comprehensive way. Here, we show that a manifold learning approach can coarse grain bacterial communities in terms of their metabolic strategies and that we can thereby quantitatively organize genomic information in terms of potentially occupied niches over time. This approach, therefore, advances our understanding of how fluctuations in bacterial abundances and species composition can relate to ecosystem functions and it can facilitate the analysis, monitoring, and future predictions of the development of microbial communities. American Society for Microbiology 2023-05-31 /pmc/articles/PMC10312292/ /pubmed/37255288 http://dx.doi.org/10.1128/msystems.00028-23 Text en Copyright © 2023 Massing et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Massing, Jana C
Fahimipour, Ashkaan K.
Bunse, Carina
Pinhassi, Jarone
Gross, Thilo
Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title_full Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title_fullStr Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title_full_unstemmed Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title_short Quantification of metabolic niche occupancy dynamics in a Baltic Sea bacterial community
title_sort quantification of metabolic niche occupancy dynamics in a baltic sea bacterial community
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10312292/
https://www.ncbi.nlm.nih.gov/pubmed/37255288
http://dx.doi.org/10.1128/msystems.00028-23
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