Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation.

Clare Bird,Anders Meibom,Emmanuelle Geslin,Charlotte Lekieffre,Ann D Russell,Helena L Filipsson,Olivier Maire,Thierry Jauffrais,Jennifer S Fehrenbacher

doi:10.3389/fmicb.2020.604979

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 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.

Highlights

The nitrogen (N) cycle is one of the most complex marine biogeochemical cycles, and N exerts significant influence on the cycles of many other elements, carbon and phosphorous, because it is often among the elements that can limit biological productivity (Gruber, 2008)
The cytoplasm of Ammonia sp. exhibited typical organelles observed in other benthic species (LeKieffre et al, 2018a): lipid droplets, organic lining, residual bodies, electron-opaque bodies (200–500 nm circular inclusions), fibrillar vesicles, mitochondria and “empty” vacuoles (Figure 1)
In Ammonia sp. the nucleus exhibited a typical structure as described in previous studies (LeKieffre et al, 2018a), with a double membrane and several nucleoli scattered in the nucleoplasm (Figure 3)

Summary

Introduction

The nitrogen (N) cycle is one of the most complex marine biogeochemical cycles, and N exerts significant influence on the cycles of many other elements, carbon and phosphorous, because it is often among the elements that can limit biological productivity (Gruber, 2008). Benthic foraminifera are heterotrophic protists that inhabit the marine sediments ranging from salt marshes and intertidal zones to the deep-sea trenches (Murray, 2006), and planktonic foraminifera occupy all open ocean surface waters, occasionally down to 4,000 m (Schiebel and Hemleben, 2017). Their diets vary, but include phytodetritus, bacteria, algae, phyto- and zooplankton, and nematodes (Moodley et al, 2000; Pascal et al, 2008; Dupuy et al, 2010; Enge et al, 2016; Bird et al, 2017, 2018; Chronopoulou et al, 2019). Some species are mixotrophic (Mitra et al, 2016); they house algal symbionts (Gastrich, 1987; Spero, 1987) or kleptoplasts (Jauffrais et al, 2018) that provide fixed carbon to the host whilst maintaining a heterotrophic mode of feeding (Jauffrais et al, 2016; LeKieffre et al, 2018b)

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Results

Discussion

Conclusion