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Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer

Haynesina germanica, an ubiquitous benthic foraminifer in intertidal mudflats, has the remarkable ability to isolate, sequester, and use chloroplasts from microalgae. The photosynthetic functionality of these kleptoplasts has been demonstrated by measuring photosystem II quantum efficiency and O(2)...

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Autores principales: LeKieffre, Charlotte, Jauffrais, Thierry, Geslin, Emmanuelle, Jesus, Bruno, Bernhard, Joan M., Giovani, Maria-Evangelia, Meibom, Anders
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6031614/
https://www.ncbi.nlm.nih.gov/pubmed/29973634
http://dx.doi.org/10.1038/s41598-018-28455-1
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author LeKieffre, Charlotte
Jauffrais, Thierry
Geslin, Emmanuelle
Jesus, Bruno
Bernhard, Joan M.
Giovani, Maria-Evangelia
Meibom, Anders
author_facet LeKieffre, Charlotte
Jauffrais, Thierry
Geslin, Emmanuelle
Jesus, Bruno
Bernhard, Joan M.
Giovani, Maria-Evangelia
Meibom, Anders
author_sort LeKieffre, Charlotte
collection PubMed
description Haynesina germanica, an ubiquitous benthic foraminifer in intertidal mudflats, has the remarkable ability to isolate, sequester, and use chloroplasts from microalgae. The photosynthetic functionality of these kleptoplasts has been demonstrated by measuring photosystem II quantum efficiency and O(2) production rates, but the precise role of the kleptoplasts in foraminiferal metabolism is poorly understood. Thus, the mechanism and dynamics of C and N assimilation and translocation from the kleptoplasts to the foraminiferal host requires study. The objective of this study was to investigate, using correlated TEM and NanoSIMS imaging, the assimilation of inorganic C and N (here ammonium, NH(4)(+)) in individuals of a kleptoplastic benthic foraminiferal species. H. germanica specimens were incubated for 20 h in artificial seawater enriched with H(13)CO(3)(−) and (15)NH(4)(+) during a light/dark cycle. All specimens (n = 12) incorporated (13)C into their endoplasm stored primarily in the form of lipid droplets. A control incubation in darkness resulted in no (13)C-uptake, strongly suggesting that photosynthesis is the process dominating inorganic C assimilation. Ammonium assimilation was observed both with and without light, with diffuse (15)N-enrichment throughout the cytoplasm and distinct (15)N-hotspots in fibrillar vesicles, electron-opaque bodies, tubulin paracrystals, bacterial associates, and, rarely and at moderate levels, in kleptoplasts. The latter observation might indicate that the kleptoplasts are involved in N assimilation. However, the higher N assimilation observed in the foraminiferal endoplasm incubated without light suggests that another cytoplasmic pathway is dominant, at least in darkness. This study clearly shows the advantage provided by the kleptoplasts as an additional source of carbon and provides observations of ammonium uptake by the foraminiferal cell.
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spelling pubmed-60316142018-07-12 Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer LeKieffre, Charlotte Jauffrais, Thierry Geslin, Emmanuelle Jesus, Bruno Bernhard, Joan M. Giovani, Maria-Evangelia Meibom, Anders Sci Rep Article Haynesina germanica, an ubiquitous benthic foraminifer in intertidal mudflats, has the remarkable ability to isolate, sequester, and use chloroplasts from microalgae. The photosynthetic functionality of these kleptoplasts has been demonstrated by measuring photosystem II quantum efficiency and O(2) production rates, but the precise role of the kleptoplasts in foraminiferal metabolism is poorly understood. Thus, the mechanism and dynamics of C and N assimilation and translocation from the kleptoplasts to the foraminiferal host requires study. The objective of this study was to investigate, using correlated TEM and NanoSIMS imaging, the assimilation of inorganic C and N (here ammonium, NH(4)(+)) in individuals of a kleptoplastic benthic foraminiferal species. H. germanica specimens were incubated for 20 h in artificial seawater enriched with H(13)CO(3)(−) and (15)NH(4)(+) during a light/dark cycle. All specimens (n = 12) incorporated (13)C into their endoplasm stored primarily in the form of lipid droplets. A control incubation in darkness resulted in no (13)C-uptake, strongly suggesting that photosynthesis is the process dominating inorganic C assimilation. Ammonium assimilation was observed both with and without light, with diffuse (15)N-enrichment throughout the cytoplasm and distinct (15)N-hotspots in fibrillar vesicles, electron-opaque bodies, tubulin paracrystals, bacterial associates, and, rarely and at moderate levels, in kleptoplasts. The latter observation might indicate that the kleptoplasts are involved in N assimilation. However, the higher N assimilation observed in the foraminiferal endoplasm incubated without light suggests that another cytoplasmic pathway is dominant, at least in darkness. This study clearly shows the advantage provided by the kleptoplasts as an additional source of carbon and provides observations of ammonium uptake by the foraminiferal cell. Nature Publishing Group UK 2018-07-04 /pmc/articles/PMC6031614/ /pubmed/29973634 http://dx.doi.org/10.1038/s41598-018-28455-1 Text en © The Author(s) 2018 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
LeKieffre, Charlotte
Jauffrais, Thierry
Geslin, Emmanuelle
Jesus, Bruno
Bernhard, Joan M.
Giovani, Maria-Evangelia
Meibom, Anders
Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title_full Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title_fullStr Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title_full_unstemmed Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title_short Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
title_sort inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6031614/
https://www.ncbi.nlm.nih.gov/pubmed/29973634
http://dx.doi.org/10.1038/s41598-018-28455-1
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