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

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 O2 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 H13CO3− and 15NH4+ during a light/dark cycle. All specimens (n = 12) incorporated 13C into their endoplasm stored primarily in the form of lipid droplets. A control incubation in darkness resulted in no 13C-uptake, strongly suggesting that photosynthesis is the process dominating inorganic C assimilation. Ammonium assimilation was observed both with and without light, with diffuse 15N-enrichment throughout the cytoplasm and distinct 15N-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.

Kleptoplastidic benthic foraminifera from aphotic habitats: insights into assimilation of inorganic C, N and S studied with sub‐cellular resolution

“…In intertidal kleptoplastidic foraminiferal species, oxygenic photosynthesis was found to be functional and inorganic carbon assimilation was demonstrated (Lopez, ; LeKieffre et al ., ). However, below the photic limit, which typically does not exceed 15–20 m in the Gullmar Fjord during the season we sampled (Erlandsson and Stigebrandt, ), it is unlikely that oxygenic photosynthesis would occur.…”

“…We combined ultrastructural analyses, which were executed with a transmission electron microscope (TEM), correlated with nanometre scale secondary ion mass spectrometry (NanoSIMS) imaging (Hoppe et al ., ; Nuñez et al ., ) to localize isotopically labelled 15 N, 13 C and 34 S compounds at a sub‐cellular level and to correlate the elemental isotopic composition with ultrastructural features of N. labradorica . This TEM‐NanoSIMS analysis has revealed the fate of isotopically labelled compounds in diverse marine microorganisms (Finzi‐Hart et al ., ; Pernice et al ., ; Kopp et al ., ; ; Raina et al ., ), including foraminifera (Nomaki et al ., ; LeKieffre et al ., ; ). Additionally, microelectrodes were used to determine the oxygen dynamics around N. labradorica as a function of artificial light exposure (Rink et al ., ; Geslin et al ., ), in order to link C and N assimilation with potential photosynthetic activity.…”

SiR-actin-labelled granules in foraminifera: patterns, dynamics, and hypotheses

“…This is due to the fact that every probe may have affinity to different epitopes of Factin, therefore, may not label all different F-actin-containing structures equally. The effectiveness of staining F-actin using different probes was compared by Lemieux et al (2014). They reported that different probes did not stain all subsets of F-actin equally.…”

Dynamics and organization of actin-labelled granules as a rapid transport mode of actin cytoskeleton components in Foraminifera

“…Although the chemical composition of FV is uncertain we can assume from a high content of nitrogen (LeKieffre et al, 2018b) that they likely contain proteins. Internal material contained within FV appears to have a specific 3D net-like nanostructure.…”