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Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom

BACKGROUND: Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that collectively remineralize gigatons of algal biomass on a global scale. This biomass is largely composed of distinct polysacchar...

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Autores principales: Sidhu, Chandni, Kirstein, Inga V., Meunier, Cédric L., Rick, Johannes, Fofonova, Vera, Wiltshire, Karen H., Steinke, Nicola, Vidal-Melgosa, Silvia, Hehemann, Jan-Hendrik, Huettel, Bruno, Schweder, Thomas, Fuchs, Bernhard M., Amann, Rudolf I., Teeling, Hanno
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10108472/
https://www.ncbi.nlm.nih.gov/pubmed/37069671
http://dx.doi.org/10.1186/s40168-023-01517-x
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author Sidhu, Chandni
Kirstein, Inga V.
Meunier, Cédric L.
Rick, Johannes
Fofonova, Vera
Wiltshire, Karen H.
Steinke, Nicola
Vidal-Melgosa, Silvia
Hehemann, Jan-Hendrik
Huettel, Bruno
Schweder, Thomas
Fuchs, Bernhard M.
Amann, Rudolf I.
Teeling, Hanno
author_facet Sidhu, Chandni
Kirstein, Inga V.
Meunier, Cédric L.
Rick, Johannes
Fofonova, Vera
Wiltshire, Karen H.
Steinke, Nicola
Vidal-Melgosa, Silvia
Hehemann, Jan-Hendrik
Huettel, Bruno
Schweder, Thomas
Fuchs, Bernhard M.
Amann, Rudolf I.
Teeling, Hanno
author_sort Sidhu, Chandni
collection PubMed
description BACKGROUND: Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that collectively remineralize gigatons of algal biomass on a global scale. This biomass is largely composed of distinct polysaccharides, and the microbial decomposition of these polysaccharides is therefore a process of prime importance. RESULTS: In 2020, we sampled a complete biphasic spring bloom in the German Bight over a 90-day period. Bacterioplankton metagenomes from 30 time points allowed reconstruction of 251 metagenome-assembled genomes (MAGs). Corresponding metatranscriptomes highlighted 50 particularly active MAGs of the most abundant clades, including many polysaccharide degraders. Saccharide measurements together with bacterial polysaccharide utilization loci (PUL) expression data identified β-glucans (diatom laminarin) and α-glucans as the most prominent and actively metabolized dissolved polysaccharide substrates. Both substrates were consumed throughout the bloom, with α-glucan PUL expression peaking at the beginning of the second bloom phase shortly after a peak in flagellate and the nadir in bacterial total cell counts. CONCLUSIONS: We show that the amounts and composition of dissolved polysaccharides, in particular abundant storage polysaccharides, have a pronounced influence on the composition of abundant bacterioplankton members during phytoplankton blooms, some of which compete for similar polysaccharide niches. We hypothesize that besides the release of algal glycans, also recycling of bacterial glycans as a result of increased bacterial cell mortality can have a significant influence on bacterioplankton composition during phytoplankton blooms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01517-x.
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spelling pubmed-101084722023-04-18 Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom Sidhu, Chandni Kirstein, Inga V. Meunier, Cédric L. Rick, Johannes Fofonova, Vera Wiltshire, Karen H. Steinke, Nicola Vidal-Melgosa, Silvia Hehemann, Jan-Hendrik Huettel, Bruno Schweder, Thomas Fuchs, Bernhard M. Amann, Rudolf I. Teeling, Hanno Microbiome Research BACKGROUND: Blooms of marine microalgae play a pivotal role in global carbon cycling. Such blooms entail successive blooms of specialized clades of planktonic bacteria that collectively remineralize gigatons of algal biomass on a global scale. This biomass is largely composed of distinct polysaccharides, and the microbial decomposition of these polysaccharides is therefore a process of prime importance. RESULTS: In 2020, we sampled a complete biphasic spring bloom in the German Bight over a 90-day period. Bacterioplankton metagenomes from 30 time points allowed reconstruction of 251 metagenome-assembled genomes (MAGs). Corresponding metatranscriptomes highlighted 50 particularly active MAGs of the most abundant clades, including many polysaccharide degraders. Saccharide measurements together with bacterial polysaccharide utilization loci (PUL) expression data identified β-glucans (diatom laminarin) and α-glucans as the most prominent and actively metabolized dissolved polysaccharide substrates. Both substrates were consumed throughout the bloom, with α-glucan PUL expression peaking at the beginning of the second bloom phase shortly after a peak in flagellate and the nadir in bacterial total cell counts. CONCLUSIONS: We show that the amounts and composition of dissolved polysaccharides, in particular abundant storage polysaccharides, have a pronounced influence on the composition of abundant bacterioplankton members during phytoplankton blooms, some of which compete for similar polysaccharide niches. We hypothesize that besides the release of algal glycans, also recycling of bacterial glycans as a result of increased bacterial cell mortality can have a significant influence on bacterioplankton composition during phytoplankton blooms. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40168-023-01517-x. BioMed Central 2023-04-17 /pmc/articles/PMC10108472/ /pubmed/37069671 http://dx.doi.org/10.1186/s40168-023-01517-x Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Sidhu, Chandni
Kirstein, Inga V.
Meunier, Cédric L.
Rick, Johannes
Fofonova, Vera
Wiltshire, Karen H.
Steinke, Nicola
Vidal-Melgosa, Silvia
Hehemann, Jan-Hendrik
Huettel, Bruno
Schweder, Thomas
Fuchs, Bernhard M.
Amann, Rudolf I.
Teeling, Hanno
Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title_full Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title_fullStr Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title_full_unstemmed Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title_short Dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a North Sea spring phytoplankton bloom
title_sort dissolved storage glycans shaped the community composition of abundant bacterioplankton clades during a north sea spring phytoplankton bloom
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10108472/
https://www.ncbi.nlm.nih.gov/pubmed/37069671
http://dx.doi.org/10.1186/s40168-023-01517-x
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