Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

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.


nitrogen cycle, heterotrophic protists, foraminifera, ammonium assimilation, heterotrophy, marine

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Table 1 | Sampling information and experimental manipulations for each foraminiferal specimen collected.
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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. ..
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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...
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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.
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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.). https://doi.org/10.3389/fmicb.2020.604979, https://archimer.ifremer.fr/doc/00662/77421/

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