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Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

Bird, Clare ; LeKieffre, Charlotte ; Jauffrais, Thierry ; Meibom, Anders ; Geslin, Emmanuelle ; Filipsson, Helena L. LU orcid ; Maire, Olivier ; Russell, Ann D. and Fehrenbacher, Jennifer S. (2020) In Frontiers in Microbiology 11.
Abstract

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... (More)

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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organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
ammonium assimilation, foraminifera, heterotrophic protists, heterotrophy, marine, nitrogen cycle
in
Frontiers in Microbiology
volume
11
article number
604979
publisher
Frontiers Media S. A.
external identifiers
  • scopus:85097733190
  • pmid:33343548
ISSN
1664-302X
DOI
10.3389/fmicb.2020.604979
language
English
LU publication?
yes
id
0293a234-452c-435f-be27-892a342d896b
date added to LUP
2021-01-05 14:19:56
date last changed
2025-03-07 06:12:13
@article{0293a234-452c-435f-be27-892a342d896b,
  abstract     = {{<p>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 (<sup>15</sup>N-ammonium and <sup>13</sup>C-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 <sup>13</sup>C-bicarbonate. However, both species assimilated dissolved <sup>15</sup>N-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.</p>}},
  author       = {{Bird, Clare and LeKieffre, Charlotte and Jauffrais, Thierry and Meibom, Anders and Geslin, Emmanuelle and Filipsson, Helena L. and Maire, Olivier and Russell, Ann D. and Fehrenbacher, Jennifer S.}},
  issn         = {{1664-302X}},
  keywords     = {{ammonium assimilation; foraminifera; heterotrophic protists; heterotrophy; marine; nitrogen cycle}},
  language     = {{eng}},
  publisher    = {{Frontiers Media S. A.}},
  series       = {{Frontiers in Microbiology}},
  title        = {{Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation}},
  url          = {{http://dx.doi.org/10.3389/fmicb.2020.604979}},
  doi          = {{10.3389/fmicb.2020.604979}},
  volume       = {{11}},
  year         = {{2020}},
}