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Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities

Ammonium is a central nutrient in aquatic systems. Yet, cell-specific ammonium assimilation among diverse functional plankton is poorly documented in field communities. Combining stable-isotope incubations ((15)N-ammonium, (15)N(2) and (13)C-bicarbonate) with secondary-ion mass spectrometry, we quan...

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Autores principales: Klawonn, Isabell, Bonaglia, Stefano, Whitehouse, Martin J., Littmann, Sten, Tienken, Daniela, Kuypers, Marcel M. M., Brüchert, Volker, Ploug, Helle
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776039/
https://www.ncbi.nlm.nih.gov/pubmed/30911131
http://dx.doi.org/10.1038/s41396-019-0386-z
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author Klawonn, Isabell
Bonaglia, Stefano
Whitehouse, Martin J.
Littmann, Sten
Tienken, Daniela
Kuypers, Marcel M. M.
Brüchert, Volker
Ploug, Helle
author_facet Klawonn, Isabell
Bonaglia, Stefano
Whitehouse, Martin J.
Littmann, Sten
Tienken, Daniela
Kuypers, Marcel M. M.
Brüchert, Volker
Ploug, Helle
author_sort Klawonn, Isabell
collection PubMed
description Ammonium is a central nutrient in aquatic systems. Yet, cell-specific ammonium assimilation among diverse functional plankton is poorly documented in field communities. Combining stable-isotope incubations ((15)N-ammonium, (15)N(2) and (13)C-bicarbonate) with secondary-ion mass spectrometry, we quantified bulk ammonium dynamics, N(2)-fixation and carbon (C) fixation, as well as single-cell ammonium assimilation and C-fixation within plankton communities in nitrogen (N)-depleted surface waters during summer in the Baltic Sea. Ammonium production resulted from regenerated (≥91%) and new production (N(2)-fixation, ≤9%), supporting primary production by 78–97 and 2–16%, respectively. Ammonium was produced and consumed at balanced rates, and rapidly recycled within 1 h, as shown previously, facilitating an efficient ammonium transfer within plankton communities. N(2)-fixing cyanobacteria poorly assimilated ammonium, whereas heterotrophic bacteria and picocyanobacteria accounted for its highest consumption (~20 and ~20–40%, respectively). Surprisingly, ammonium assimilation and C-fixation were similarly fast for picocyanobacteria (non-N(2)-fixing Synechococcus) and large diatoms (Chaetoceros). Yet, the population biomass was high for Synechococcus but low for Chaetoceros. Hence, autotrophic picocyanobacteria and heterotrophic bacteria, with their high single-cell assimilation rates and dominating population biomass, competed for the same nutrient source and drove rapid ammonium dynamics in N-depleted marine waters.
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spelling pubmed-67760392019-10-04 Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities Klawonn, Isabell Bonaglia, Stefano Whitehouse, Martin J. Littmann, Sten Tienken, Daniela Kuypers, Marcel M. M. Brüchert, Volker Ploug, Helle ISME J Article Ammonium is a central nutrient in aquatic systems. Yet, cell-specific ammonium assimilation among diverse functional plankton is poorly documented in field communities. Combining stable-isotope incubations ((15)N-ammonium, (15)N(2) and (13)C-bicarbonate) with secondary-ion mass spectrometry, we quantified bulk ammonium dynamics, N(2)-fixation and carbon (C) fixation, as well as single-cell ammonium assimilation and C-fixation within plankton communities in nitrogen (N)-depleted surface waters during summer in the Baltic Sea. Ammonium production resulted from regenerated (≥91%) and new production (N(2)-fixation, ≤9%), supporting primary production by 78–97 and 2–16%, respectively. Ammonium was produced and consumed at balanced rates, and rapidly recycled within 1 h, as shown previously, facilitating an efficient ammonium transfer within plankton communities. N(2)-fixing cyanobacteria poorly assimilated ammonium, whereas heterotrophic bacteria and picocyanobacteria accounted for its highest consumption (~20 and ~20–40%, respectively). Surprisingly, ammonium assimilation and C-fixation were similarly fast for picocyanobacteria (non-N(2)-fixing Synechococcus) and large diatoms (Chaetoceros). Yet, the population biomass was high for Synechococcus but low for Chaetoceros. Hence, autotrophic picocyanobacteria and heterotrophic bacteria, with their high single-cell assimilation rates and dominating population biomass, competed for the same nutrient source and drove rapid ammonium dynamics in N-depleted marine waters. Nature Publishing Group UK 2019-03-25 2019-08 /pmc/articles/PMC6776039/ /pubmed/30911131 http://dx.doi.org/10.1038/s41396-019-0386-z Text en © The Author(s) 2019 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/.
spellingShingle Article
Klawonn, Isabell
Bonaglia, Stefano
Whitehouse, Martin J.
Littmann, Sten
Tienken, Daniela
Kuypers, Marcel M. M.
Brüchert, Volker
Ploug, Helle
Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title_full Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title_fullStr Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title_full_unstemmed Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title_short Untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
title_sort untangling hidden nutrient dynamics: rapid ammonium cycling and single-cell ammonium assimilation in marine plankton communities
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6776039/
https://www.ncbi.nlm.nih.gov/pubmed/30911131
http://dx.doi.org/10.1038/s41396-019-0386-z
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