Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

Type Article
Date 2020-12
Language English
Author(s) Bird Clare1, 2, Lekieffre Charlotte3, 4, Jauffrais ThierryORCID5, Meibom Anders3, 6, Geslin Emmanuelle4, Filipsson Helena L.7, Maire Olivier8, 9, Russell Ann D.10, Fehrenbacher Jennifer S.11
Affiliation(s) 1 : Biological and Environmental Sciences, Faculty of Natural Sciences, University of Stirling, Stirling, United Kingdom
2 : School of GeoSciences, Grant Institute, University of Edinburgh, Edinburgh, United Kingdom
3 : Laboratory for Biological Geochemistry, School of Architecture, Civil and Environmental Engineering (ENAC), Ecole Polytechnique Fédérale de Lausanne (EPFL), Lausanne, Switzerland
4 : UMR CNRS 6112 LPG, Bio-Indicateurs Actuels et Fossiles, Université d’Angers, Angers, France
5 : Ifremer, IRD, Univ Nouvelle–Calédonie, Univ La Réunion, CNRS, UMR 9220 ENTROPIE, Nouméa, New Caledonia
6 : Centre for Advanced Surface Analysis, Institute of Earth Sciences, University of Lausanne, Lausanne, Switzerland
7 : Department of Geology, Lund University, Lund, Sweden
8 : Université de Bordeaux, EPOC, UMR 5805, Talence, France
9 : CNRS, EPOC, UMR 5805, Talence, France
10 : Department of Earth and Planetary Sciences, University of California, Davis, Davis, CA, United States
11 : College of Earth, Ocean, and Atmospheric Sciences, Oregon State University, Corvallis, OR, United States
Source Frontiers In Microbiology (1664-302X) (Frontiers Media SA), 2020-12 , Vol. 11 , P. 604979 (13p.)
DOI 10.3389/fmicb.2020.604979
WOS© Times Cited 5
Keyword(s) nitrogen cycle, heterotrophic protists, foraminifera, ammonium assimilation, heterotrophy, marine

Nitrogen availability often limits biological productivity in marine systems, where inorganic nitrogen, such as ammonium is assimilated into the food web by bacteria and photoautotrophic eukaryotes. Recently, ammonium assimilation was observed in kleptoplast-containing protists of the phylum foraminifera, possibly via the glutamine synthetase/glutamate synthase (GS/GOGAT) assimilation pathway imported with the kleptoplasts. However, it is not known if the ubiquitous and diverse heterotrophic protists have an innate ability for ammonium assimilation. Using stable isotope incubations (15N-ammonium and 13C-bicarbonate) and combining transmission electron microscopy (TEM) with quantitative nanoscale secondary ion mass spectrometry (NanoSIMS) imaging, we investigated the uptake and assimilation of dissolved inorganic ammonium by two heterotrophic foraminifera; a non-kleptoplastic benthic species, Ammonia sp., and a planktonic species, Globigerina bulloides. These species are heterotrophic and not capable of photosynthesis. Accordingly, they did not assimilate 13C-bicarbonate. However, both species assimilated dissolved 15N-ammonium and incorporated it into organelles of direct importance for ontogenetic growth and development of the cell. These observations demonstrate that at least some heterotrophic protists have an innate cellular mechanism for inorganic ammonium assimilation, highlighting a newly discovered pathway for dissolved inorganic nitrogen (DIN) assimilation within the marine microbial loop.

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Publisher's official version 13 6 MB Open access
Table 1 | Sampling information and experimental manipulations for each foraminiferal specimen collected. 16 KB Open access
Table 2 | Excel spreadsheet of raw data with means and SDs of natural isotopic δ13C and δ15N values and 15N enrichments in regions of interest (ROIs) in different sub-cellular structures within G. .. 30 KB Open access
Figure 1 | Representative ion counts for the ions 12C12C–, 13C12C–-, 12C14N–, and 12C15N– for the species Ammonia sp. and G. bulloides obtained after drift correction and accumulation of the six to... 6 MB Open access
Figure 2 | 15N cellular localization in the electron-opaque bodies and fibrillar vesicles of G. bulloides after 6 h. Arrows: electron-opaque bodies; circles: fibrillar vesicles. 1 MB Open access
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How to cite 

Bird Clare, Lekieffre Charlotte, Jauffrais Thierry, Meibom Anders, Geslin Emmanuelle, Filipsson Helena L., Maire Olivier, Russell Ann D., Fehrenbacher Jennifer S. (2020). Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation. Frontiers In Microbiology, 11, 604979 (13p.). Publisher's official version : https://doi.org/10.3389/fmicb.2020.604979 , Open Access version : https://archimer.ifremer.fr/doc/00662/77421/