Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera
LeKieffre, Charlotte ; Jauffrais, Thierry LU ; Bernhard, Joan M. ; Filipsson, Helena L. LU
; Schmidt, Christiane
; Roberge, Hélène
; Maire, Olivier
; Panieri, Giuliana
; Geslin, Emmanuelle
and Meibom, Anders
(2022)
In Frontiers in Marine Science
9.
- Abstract
Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used... (More)
Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable 15N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding 15N and 34S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.
(Less)
- author
- LeKieffre, Charlotte
; Jauffrais, Thierry
LU
; Bernhard, Joan M.
; Filipsson, Helena L.
LU
; Schmidt, Christiane
; Roberge, Hélène
; Maire, Olivier
; Panieri, Giuliana
; Geslin, Emmanuelle
and Meibom, Anders
- organization
- publishing date
- 2022-07-20
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- biogeochemical cycles, coastal environments, marine protists, NanoSIMS, nitrogen, sulfur
- in
- Frontiers in Marine Science
- volume
- 9
- article number
- 861945
- pages
- 10 pages
- publisher
- Frontiers Media S. A.
- external identifiers
-
- scopus:85135465102
- ISSN
- 2296-7745
- DOI
- 10.3389/fmars.2022.861945
- language
- English
- LU publication?
- yes
- additional info
- Funding Information: This work was supported by the Swiss National Science Foundation (grant no. 200021_149333), and a postdoctoral fellowship allowed to CL by the University Loire-Bretagne. SBB sampling was funded by US National Science Foundation grant BIO IOS 1557430 to JMB, who also acknowledges NASA grant #80NSSC21K0478 for partial support. HF acknowledges funding from the Swedish Research Council VR (grant number 2017-04190). Svalbard sampling was supported by the Research Council of Norway through CAGE (Center for Excellence in Arctic Gas Hydrate Environment and Climate, project number 223259) and NORCRUST (project number 255150) to GP and the fellowship MOPGA (Make Our Planet Great Again) by CAMPUS France to CS. Funding Information: Florence Manero from the SCIAM platform at the University of Angers (France), the electron microscopy facility (EMF) at the University of Lausanne (Switzerland), the crews of the R/V Skagerak, R/V Kronprins Haakon, R/V Robert Gordon Sproul and ROV Ægir team are thanked for help and technical assistance. Inda Brinkmann, Constance Choquel, Sami Jokinen, Aurélia Mouret and Hanna Nilsson are thanked for their help with foraminiferal sampling in the Gullmar Fjord. Stephane Escrig is thanked for expertise and help with NanoSIMS imaging. Publisher Copyright: Copyright © 2022 LeKieffre, Jauffrais, Bernhard, Filipsson, Schmidt, Roberge, Maire, Panieri, Geslin and Meibom.
- id
- 914671ba-81bb-4970-87a5-5360f47b66b0
- date added to LUP
- 2022-08-17 22:08:13
- date last changed
- 2023-05-10 11:23:31
@article{914671ba-81bb-4970-87a5-5360f47b66b0,
abstract = {{<p>Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable <sup>15</sup>N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding <sup>15</sup>N and <sup>34</sup>S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.</p>}},
author = {{LeKieffre, Charlotte and Jauffrais, Thierry and Bernhard, Joan M. and Filipsson, Helena L. and Schmidt, Christiane and Roberge, Hélène and Maire, Olivier and Panieri, Giuliana and Geslin, Emmanuelle and Meibom, Anders}},
issn = {{2296-7745}},
keywords = {{biogeochemical cycles; coastal environments; marine protists; NanoSIMS; nitrogen; sulfur}},
language = {{eng}},
month = {{07}},
publisher = {{Frontiers Media S. A.}},
series = {{Frontiers in Marine Science}},
title = {{Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera}},
url = {{http://dx.doi.org/10.3389/fmars.2022.861945}},
doi = {{10.3389/fmars.2022.861945}},
volume = {{9}},
year = {{2022}},
}