Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera
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-...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-07-01
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| Series: | Frontiers in Marine Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fmars.2022.861945/full |
| _version_ | 1817971009954775040 |
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| author | Charlotte LeKieffre Charlotte LeKieffre Thierry Jauffrais Joan M. Bernhard Helena L. Filipsson Christiane Schmidt Christiane Schmidt Hélène Roberge Olivier Maire Giuliana Panieri Emmanuelle Geslin Anders Meibom Anders Meibom |
| author_facet | Charlotte LeKieffre Charlotte LeKieffre Thierry Jauffrais Joan M. Bernhard Helena L. Filipsson Christiane Schmidt Christiane Schmidt Hélène Roberge Olivier Maire Giuliana Panieri Emmanuelle Geslin Anders Meibom Anders Meibom |
| author_sort | Charlotte LeKieffre |
| collection | DOAJ |
| description | 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. |
| first_indexed | 2024-04-13T20:41:22Z |
| format | Article |
| id | doaj.art-2031ba35af624388bff091831246ec48 |
| institution | Directory Open Access Journal |
| issn | 2296-7745 |
| language | English |
| last_indexed | 2024-04-13T20:41:22Z |
| publishDate | 2022-07-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Marine Science |
| spelling | doaj.art-2031ba35af624388bff091831246ec482022-12-22T02:30:50ZengFrontiers Media S.A.Frontiers in Marine Science2296-77452022-07-01910.3389/fmars.2022.861945861945Ammonium and Sulfate Assimilation Is Widespread in Benthic ForaminiferaCharlotte LeKieffre0Charlotte LeKieffre1Thierry Jauffrais2Joan M. Bernhard3Helena L. Filipsson4Christiane Schmidt5Christiane Schmidt6Hélène Roberge7Olivier Maire8Giuliana Panieri9Emmanuelle Geslin10Anders Meibom11Anders Meibom12LPG UMR 6112, Univ Angers, Nantes Université, Le Mans Univ, CNRS, Angers, FranceLaboratory for Biological Geochemistry, School of Architecture, Civil- and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandIfremer, IRD, Univ. Nouvelle-Calédonie, Univ. La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New CaledoniaGeology and Geophysics Department, Woods Hole Oceanographic Institution, Woods Hole, MA, United StatesDepartment of Geology, Lund University, Lund, SwedenLPG UMR 6112, Univ Angers, Nantes Université, Le Mans Univ, CNRS, Angers, FranceCentre for Arctic Gas Hydrate, Environment and Climate (CAGE), Department of Geosciences, UiT The Arctic University of Norway, Tromsø, NorwayLPG UMR 6112, Univ Angers, Nantes Université, Le Mans Univ, CNRS, Angers, FranceUniv. Bordeaux, EPOC, UMR 5805 CNRS, OASU, Arcachon, FranceCentre for Arctic Gas Hydrate, Environment and Climate (CAGE), Department of Geosciences, UiT The Arctic University of Norway, Tromsø, NorwayLPG UMR 6112, Univ Angers, Nantes Université, Le Mans Univ, CNRS, Angers, FranceLaboratory for Biological Geochemistry, School of Architecture, Civil- and Environmental Engineering, Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, SwitzerlandCenter for Advanced Surface Science (CASA), Institute of Earth Sciences, University of Lausanne, Lausanne, SwitzerlandNitrogen 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.https://www.frontiersin.org/articles/10.3389/fmars.2022.861945/fullmarine protistscoastal environmentsbiogeochemical cyclesNanoSIMSnitrogensulfur |
| spellingShingle | Charlotte LeKieffre Charlotte LeKieffre Thierry Jauffrais Joan M. Bernhard Helena L. Filipsson Christiane Schmidt Christiane Schmidt Hélène Roberge Olivier Maire Giuliana Panieri Emmanuelle Geslin Anders Meibom Anders Meibom Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera Frontiers in Marine Science marine protists coastal environments biogeochemical cycles NanoSIMS nitrogen sulfur |
| title | Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera |
| title_full | Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera |
| title_fullStr | Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera |
| title_full_unstemmed | Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera |
| title_short | Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera |
| title_sort | ammonium and sulfate assimilation is widespread in benthic foraminifera |
| topic | marine protists coastal environments biogeochemical cycles NanoSIMS nitrogen sulfur |
| url | https://www.frontiersin.org/articles/10.3389/fmars.2022.861945/full |
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