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Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system

Coastal upwelling zones are hotspots of oceanic productivity, driven by phytoplankton photosynthesis. Bacteria, in turn, grow on and are the principal remineralizers of dissolved organic matter (DOM) produced in aquatic ecosystems. However, the molecular processes that key bacterial taxa employ to r...

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Autores principales: Pontiller, Benjamin, Martínez-García, Sandra, Joglar, Vanessa, Amnebrink, Dennis, Pérez-Martínez, Clara, González, José M., Lundin, Daniel, Fernández, Emilio, Teira, Eva, Pinhassi, Jarone
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9478159/
https://www.ncbi.nlm.nih.gov/pubmed/35804052
http://dx.doi.org/10.1038/s41396-022-01273-0
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author Pontiller, Benjamin
Martínez-García, Sandra
Joglar, Vanessa
Amnebrink, Dennis
Pérez-Martínez, Clara
González, José M.
Lundin, Daniel
Fernández, Emilio
Teira, Eva
Pinhassi, Jarone
author_facet Pontiller, Benjamin
Martínez-García, Sandra
Joglar, Vanessa
Amnebrink, Dennis
Pérez-Martínez, Clara
González, José M.
Lundin, Daniel
Fernández, Emilio
Teira, Eva
Pinhassi, Jarone
author_sort Pontiller, Benjamin
collection PubMed
description Coastal upwelling zones are hotspots of oceanic productivity, driven by phytoplankton photosynthesis. Bacteria, in turn, grow on and are the principal remineralizers of dissolved organic matter (DOM) produced in aquatic ecosystems. However, the molecular processes that key bacterial taxa employ to regulate the turnover of phytoplankton-derived DOM are not well understood. We therefore carried out comparative time-series metatranscriptome analyses of bacterioplankton in the Northwest Iberian upwelling system, using parallel sampling of seawater and mesocosms with in situ-like conditions. The mesocosm experiment uncovered a taxon-specific progression of transcriptional responses from bloom development (characterized by a diverse set of taxa in the orders Cellvibrionales, Rhodobacterales, and Pelagibacterales), over early decay (mainly taxa in the Alteromonadales and Flavobacteriales), to senescence phases (Flavobacteriales and Saprospirales taxa). Pronounced order-specific differences in the transcription of glycoside hydrolases, peptidases, and transporters were found, supporting that functional resource partitioning is dynamically structured by temporal changes in available DOM. In addition, comparative analysis of mesocosm and field samples revealed a high degree of metabolic plasticity in the degradation and uptake of carbohydrates and nitrogen-rich compounds, suggesting these gene systems critically contribute to modulating the stoichiometry of the labile DOM pool. Our findings suggest that cascades of transcriptional responses in gene systems for the utilization of organic matter and nutrients largely shape the fate of organic matter on the time scales typical of upwelling-driven phytoplankton blooms.
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spelling pubmed-94781592022-09-17 Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system Pontiller, Benjamin Martínez-García, Sandra Joglar, Vanessa Amnebrink, Dennis Pérez-Martínez, Clara González, José M. Lundin, Daniel Fernández, Emilio Teira, Eva Pinhassi, Jarone ISME J Article Coastal upwelling zones are hotspots of oceanic productivity, driven by phytoplankton photosynthesis. Bacteria, in turn, grow on and are the principal remineralizers of dissolved organic matter (DOM) produced in aquatic ecosystems. However, the molecular processes that key bacterial taxa employ to regulate the turnover of phytoplankton-derived DOM are not well understood. We therefore carried out comparative time-series metatranscriptome analyses of bacterioplankton in the Northwest Iberian upwelling system, using parallel sampling of seawater and mesocosms with in situ-like conditions. The mesocosm experiment uncovered a taxon-specific progression of transcriptional responses from bloom development (characterized by a diverse set of taxa in the orders Cellvibrionales, Rhodobacterales, and Pelagibacterales), over early decay (mainly taxa in the Alteromonadales and Flavobacteriales), to senescence phases (Flavobacteriales and Saprospirales taxa). Pronounced order-specific differences in the transcription of glycoside hydrolases, peptidases, and transporters were found, supporting that functional resource partitioning is dynamically structured by temporal changes in available DOM. In addition, comparative analysis of mesocosm and field samples revealed a high degree of metabolic plasticity in the degradation and uptake of carbohydrates and nitrogen-rich compounds, suggesting these gene systems critically contribute to modulating the stoichiometry of the labile DOM pool. Our findings suggest that cascades of transcriptional responses in gene systems for the utilization of organic matter and nutrients largely shape the fate of organic matter on the time scales typical of upwelling-driven phytoplankton blooms. Nature Publishing Group UK 2022-07-08 2022-10 /pmc/articles/PMC9478159/ /pubmed/35804052 http://dx.doi.org/10.1038/s41396-022-01273-0 Text en © The Author(s) 2022 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
Pontiller, Benjamin
Martínez-García, Sandra
Joglar, Vanessa
Amnebrink, Dennis
Pérez-Martínez, Clara
González, José M.
Lundin, Daniel
Fernández, Emilio
Teira, Eva
Pinhassi, Jarone
Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title_full Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title_fullStr Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title_full_unstemmed Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title_short Rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
title_sort rapid bacterioplankton transcription cascades regulate organic matter utilization during phytoplankton bloom progression in a coastal upwelling system
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9478159/
https://www.ncbi.nlm.nih.gov/pubmed/35804052
http://dx.doi.org/10.1038/s41396-022-01273-0
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