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

Type Article
Date 2018-07
Language English
Author(s) Lekieffre Charlotte1, 2, Jauffrais ThierryORCID2, Geslin Emmanuelle2, Jesus Bruno3, 4, Bernhard Joan M.5, Giovani Maria-Evangelia1, Meibom Anders1, 6
Affiliation(s) 1 : Ecole Polytech Fed Lausanne, Sch Architecture Civil & Environm Engn ENAC, Lab Biol Geochem, CH-1015 Lausanne, Switzerland.
2 : Univ Angers, UMR CNRS LPG BIAF 6112, 2 Blvd Lavoisier, F-49045 Angers 1, France.
3 : Univ Nantes, Lab Mer Mol Sante, EA2160, Nantes, France.
4 : Campo Grande Univ Lisboa, BioISI Biosyst Integrat Sci Inst, Fac Sci, Lisbon, Portugal.
5 : Woods Hole Oceanog Inst, Dept Geol & Geophys, Woods Hole, MA 02543 USA.
6 : Univ Lausanne, Inst Earth Sci, Ctr Adv Surface Anal, CH-1015 Lausanne, Switzerland.
Source Scientific Reports (2045-2322) (Nature Publishing Group), 2018-07 , Vol. 8 , N. 10140 , P. 12p.
DOI 10.1038/s41598-018-28455-1
WOS© Times Cited 19
Abstract

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, NH4+) in individuals of a kleptoplastic benthic foraminiferal species. H. germanica specimens were incubated for 20 h in artificial seawater enriched with (HCO3-)-C-13 and (NH4+)-N-15 during a light/dark cycle. All specimens (n = 12) incorporated C-13 into their endoplasm stored primarily in the form of lipid droplets. A control incubation in darkness resulted in no C-13-uptake, strongly suggesting that photosynthesis is the process dominating inorganic C assimilation. Ammonium assimilation was observed both with and without light, with diffuse N-15-enrichment throughout the cytoplasm and distinct N-15-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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Lekieffre Charlotte, Jauffrais Thierry, Geslin Emmanuelle, Jesus Bruno, Bernhard Joan M., Giovani Maria-Evangelia, Meibom Anders (2018). Inorganic carbon and nitrogen assimilation in cellular compartments of a benthic kleptoplastic foraminifer. Scientific Reports, 8(10140), 12p. Publisher's official version : https://doi.org/10.1038/s41598-018-28455-1 , Open Access version : https://archimer.ifremer.fr/doc/00457/56887/