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Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies

Trichodesmium is an important dinitrogen (N(2))-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N(2) fixation. However, rates of these transformations and co...

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Autores principales: Klawonn, Isabell, Eichner, Meri J., Wilson, Samuel T., Moradi, Nasrollah, Thamdrup, Bo, Kümmel, Steffen, Gehre, Matthias, Khalili, Arzhang, Grossart, Hans-Peter, Karl, David M., 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/PMC6976679/
https://www.ncbi.nlm.nih.gov/pubmed/31636364
http://dx.doi.org/10.1038/s41396-019-0514-9
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author Klawonn, Isabell
Eichner, Meri J.
Wilson, Samuel T.
Moradi, Nasrollah
Thamdrup, Bo
Kümmel, Steffen
Gehre, Matthias
Khalili, Arzhang
Grossart, Hans-Peter
Karl, David M.
Ploug, Helle
author_facet Klawonn, Isabell
Eichner, Meri J.
Wilson, Samuel T.
Moradi, Nasrollah
Thamdrup, Bo
Kümmel, Steffen
Gehre, Matthias
Khalili, Arzhang
Grossart, Hans-Peter
Karl, David M.
Ploug, Helle
author_sort Klawonn, Isabell
collection PubMed
description Trichodesmium is an important dinitrogen (N(2))-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N(2) fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual field-sampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N(2) fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were ~60–200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies.
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spelling pubmed-69766792020-01-23 Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies Klawonn, Isabell Eichner, Meri J. Wilson, Samuel T. Moradi, Nasrollah Thamdrup, Bo Kümmel, Steffen Gehre, Matthias Khalili, Arzhang Grossart, Hans-Peter Karl, David M. Ploug, Helle ISME J Article Trichodesmium is an important dinitrogen (N(2))-fixing cyanobacterium in marine ecosystems. Recent nucleic acid analyses indicate that Trichodesmium colonies with their diverse epibionts support various nitrogen (N) transformations beyond N(2) fixation. However, rates of these transformations and concentration gradients of N compounds in Trichodesmium colonies remain largely unresolved. We combined isotope-tracer incubations, micro-profiling and numeric modelling to explore carbon fixation, N cycling processes as well as oxygen, ammonium and nitrate concentration gradients in individual field-sampled Trichodesmium colonies. Colonies were net-autotrophic, with carbon and N(2) fixation occurring mostly during the day. Ten percent of the fixed N was released as ammonium after 12-h incubations. Nitrification was not detectable but nitrate consumption was high when nitrate was added. The consumed nitrate was partly reduced to ammonium, while denitrification was insignificant. Thus, the potential N transformation network was characterised by fixed N gain and recycling processes rather than denitrification. Oxygen concentrations within colonies were ~60–200% air-saturation. Moreover, our modelling predicted steep concentration gradients, with up to 6-fold higher ammonium concentrations, and nitrate depletion in the colony centre compared to the ambient seawater. These gradients created a chemically heterogeneous microenvironment, presumably facilitating diverse microbial metabolisms in millimetre-sized Trichodesmium colonies. Nature Publishing Group UK 2019-10-21 2020-02 /pmc/articles/PMC6976679/ /pubmed/31636364 http://dx.doi.org/10.1038/s41396-019-0514-9 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
Eichner, Meri J.
Wilson, Samuel T.
Moradi, Nasrollah
Thamdrup, Bo
Kümmel, Steffen
Gehre, Matthias
Khalili, Arzhang
Grossart, Hans-Peter
Karl, David M.
Ploug, Helle
Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title_full Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title_fullStr Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title_full_unstemmed Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title_short Distinct nitrogen cycling and steep chemical gradients in Trichodesmium colonies
title_sort distinct nitrogen cycling and steep chemical gradients in trichodesmium colonies
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6976679/
https://www.ncbi.nlm.nih.gov/pubmed/31636364
http://dx.doi.org/10.1038/s41396-019-0514-9
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