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...

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Main Authors: LeKieffre, Charlotte, Spero, Howard J, Fehrenbacher, Jennifer S, Russell, Ann D, Ren, Haojia, Geslin, Emmanuelle, Meibom, Anders
Format: Article in Journal/Newspaper
Language:unknown
Published: eScholarship, University of California 2020
Subjects:
Online Access:https://escholarship.org/uc/item/0134j5wj
id ftcdlib:oai:escholarship.org/ark:/13030/qt0134j5wj
record_format openpolar
spelling ftcdlib:oai:escholarship.org/ark:/13030/qt0134j5wj 2023-05-15T18:00:42+02:00 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 20200620 2020-06-17 application/pdf https://escholarship.org/uc/item/0134j5wj unknown eScholarship, University of California qt0134j5wj https://escholarship.org/uc/item/0134j5wj public Proceedings. Biological sciences, vol 287, iss 1929 Animals Plankton Dinoflagellida Carbon Nitrogen Ammonium Compounds Ecosystem Symbiosis Foraminifera ammonium assimilation ammonium recycling photosymbiosis dinoflagellate symbiosis planktonic foraminifera Biological Sciences Agricultural and Veterinary Sciences Medical and Health Sciences article 2020 ftcdlib 2021-01-24T17:38:05Z 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 15N-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 13C-enriched inorganic carbon, 15N-nitrate, and 15N-ammonium, as well as a 13C- and 15N- 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 15N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15N-ammonium, indicating efficient ammonium assimilation. Only weak 15N-assimilation was observed after incubation with 15N-nitrate. Feeding foraminifers with 13C- and 15N-labelled food resulted in dinoflagellates that were labelled with 15N, thereby confirming the transfer of 15N-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 δ15N 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 University of California: eScholarship
institution Open Polar
collection University of California: eScholarship
op_collection_id ftcdlib
language unknown
topic Animals
Plankton
Dinoflagellida
Carbon
Nitrogen
Ammonium Compounds
Ecosystem
Symbiosis
Foraminifera
ammonium assimilation
ammonium recycling photosymbiosis
dinoflagellate symbiosis
planktonic foraminifera
Biological Sciences
Agricultural and Veterinary Sciences
Medical and Health Sciences
spellingShingle Animals
Plankton
Dinoflagellida
Carbon
Nitrogen
Ammonium Compounds
Ecosystem
Symbiosis
Foraminifera
ammonium assimilation
ammonium recycling photosymbiosis
dinoflagellate symbiosis
planktonic foraminifera
Biological Sciences
Agricultural and Veterinary Sciences
Medical and Health Sciences
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.
topic_facet Animals
Plankton
Dinoflagellida
Carbon
Nitrogen
Ammonium Compounds
Ecosystem
Symbiosis
Foraminifera
ammonium assimilation
ammonium recycling photosymbiosis
dinoflagellate symbiosis
planktonic foraminifera
Biological Sciences
Agricultural and Veterinary Sciences
Medical and Health Sciences
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 15N-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 13C-enriched inorganic carbon, 15N-nitrate, and 15N-ammonium, as well as a 13C- and 15N- 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 15N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15N-ammonium, indicating efficient ammonium assimilation. Only weak 15N-assimilation was observed after incubation with 15N-nitrate. Feeding foraminifers with 13C- and 15N-labelled food resulted in dinoflagellates that were labelled with 15N, thereby confirming the transfer of 15N-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 δ15N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates.
format Article in Journal/Newspaper
author LeKieffre, Charlotte
Spero, Howard J
Fehrenbacher, Jennifer S
Russell, Ann D
Ren, Haojia
Geslin, Emmanuelle
Meibom, Anders
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 eScholarship, University of California
publishDate 2020
url https://escholarship.org/uc/item/0134j5wj
op_coverage 20200620
genre Planktonic foraminifera
genre_facet Planktonic foraminifera
op_source Proceedings. Biological sciences, vol 287, iss 1929
op_relation qt0134j5wj
https://escholarship.org/uc/item/0134j5wj
op_rights public
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