Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts
The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets its nitrogen (N) requirements by preying on zooplankton, and that i...
Published in: | Proceedings of the Royal Society B: Biological Sciences |
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crroyalsociety:10.1098/rspb.2020.0620 2024-06-02T08:13:26+00:00 Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts LeKieffre, Charlotte Spero, Howard J. Fehrenbacher, Jennifer S. Russell, Ann D. Ren, Haojia Geslin, Emmanuelle Meibom, Anders Swiss National Science Foundation National Science Foundation 2020 http://dx.doi.org/10.1098/rspb.2020.0620 https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2020.0620 https://royalsocietypublishing.org/doi/full-xml/10.1098/rspb.2020.0620 en eng The Royal Society http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ Proceedings of the Royal Society B: Biological Sciences volume 287, issue 1929, page 20200620 ISSN 0962-8452 1471-2954 journal-article 2020 crroyalsociety https://doi.org/10.1098/rspb.2020.0620 2024-05-07T14:16:30Z The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets its nitrogen (N) requirements by preying on zooplankton, and that its symbiotic dinoflagellates recycle metabolic ‘waste ammonium’ for their N pool. However, these conclusions were derived from bulk 15 N-enrichment experiments and model calculations, and our understanding of N assimilation and exchange between the foraminifer host cell and its symbiotic dinoflagellates remains poorly constrained. Here, we present data from pulse-chase experiments with 13 C-enriched inorganic carbon, 15 N-nitrate, and 15 N-ammonium, as well as a 13 C- and 15 N- enriched heterotrophic food source, followed by TEM (transmission electron microscopy) coupled to NanoSIMS (nanoscale secondary ion mass spectrometry) isotopic imaging to visualize and quantify C and N assimilation and translocation in the symbiotic system. High levels of 15 N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15 N-ammonium, indicating efficient ammonium assimilation. Only weak 15 N-assimilation was observed after incubation with 15 N-nitrate. Feeding foraminifers with 13 C- and 15 N-labelled food resulted in dinoflagellates that were labelled with 15 N, thereby confirming the transfer of 15 N-compounds from the digestive vacuoles of the foraminifer to the symbiotic dinoflagellates, likely through recycling of ammonium. These observations are important for N isotope-based palaeoceanographic reconstructions, as they show that δ 15 N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates. Article in Journal/Newspaper Planktonic foraminifera The Royal Society Proceedings of the Royal Society B: Biological Sciences 287 1929 20200620 |
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Open Polar |
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The Royal Society |
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crroyalsociety |
language |
English |
description |
The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets its nitrogen (N) requirements by preying on zooplankton, and that its symbiotic dinoflagellates recycle metabolic ‘waste ammonium’ for their N pool. However, these conclusions were derived from bulk 15 N-enrichment experiments and model calculations, and our understanding of N assimilation and exchange between the foraminifer host cell and its symbiotic dinoflagellates remains poorly constrained. Here, we present data from pulse-chase experiments with 13 C-enriched inorganic carbon, 15 N-nitrate, and 15 N-ammonium, as well as a 13 C- and 15 N- enriched heterotrophic food source, followed by TEM (transmission electron microscopy) coupled to NanoSIMS (nanoscale secondary ion mass spectrometry) isotopic imaging to visualize and quantify C and N assimilation and translocation in the symbiotic system. High levels of 15 N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15 N-ammonium, indicating efficient ammonium assimilation. Only weak 15 N-assimilation was observed after incubation with 15 N-nitrate. Feeding foraminifers with 13 C- and 15 N-labelled food resulted in dinoflagellates that were labelled with 15 N, thereby confirming the transfer of 15 N-compounds from the digestive vacuoles of the foraminifer to the symbiotic dinoflagellates, likely through recycling of ammonium. These observations are important for N isotope-based palaeoceanographic reconstructions, as they show that δ 15 N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates. |
author2 |
Swiss National Science Foundation National Science Foundation |
format |
Article in Journal/Newspaper |
author |
LeKieffre, Charlotte Spero, Howard J. Fehrenbacher, Jennifer S. Russell, Ann D. Ren, Haojia Geslin, Emmanuelle Meibom, Anders |
spellingShingle |
LeKieffre, Charlotte Spero, Howard J. Fehrenbacher, Jennifer S. Russell, Ann D. Ren, Haojia Geslin, Emmanuelle Meibom, Anders Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
author_facet |
LeKieffre, Charlotte Spero, Howard J. Fehrenbacher, Jennifer S. Russell, Ann D. Ren, Haojia Geslin, Emmanuelle Meibom, Anders |
author_sort |
LeKieffre, Charlotte |
title |
Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
title_short |
Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
title_full |
Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
title_fullStr |
Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
title_full_unstemmed |
Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
title_sort |
ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts |
publisher |
The Royal Society |
publishDate |
2020 |
url |
http://dx.doi.org/10.1098/rspb.2020.0620 https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2020.0620 https://royalsocietypublishing.org/doi/full-xml/10.1098/rspb.2020.0620 |
genre |
Planktonic foraminifera |
genre_facet |
Planktonic foraminifera |
op_source |
Proceedings of the Royal Society B: Biological Sciences volume 287, issue 1929, page 20200620 ISSN 0962-8452 1471-2954 |
op_rights |
http://creativecommons.org/licenses/by/4.0/ http://creativecommons.org/licenses/by/4.0/ |
op_doi |
https://doi.org/10.1098/rspb.2020.0620 |
container_title |
Proceedings of the Royal Society B: Biological Sciences |
container_volume |
287 |
container_issue |
1929 |
container_start_page |
20200620 |
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1800736949358559232 |