| 1. |
- Bird, Clare, et al.
(author)
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Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation
- 2020
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In: Frontiers in Microbiology. - : Frontiers Media SA. - 1664-302X. ; 11
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Journal article (peer-reviewed)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.
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| 2. |
- Bird, Clare, et al.
(author)
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The genetic diversity, morphology, biogeography, and taxonomic designations of Ammonia (Foraminifera) in the Northeast Atlantic
- 2020
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In: Marine Micropaleontology. - : Elsevier BV. - 0377-8398.
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Journal article (peer-reviewed)abstract
- The genetic diversity, morphology and biogeography of Ammonia specimens was investigated across the Northeast (NE) Atlantic margins, to enhance the regional (palaeo)ecological studies based on this genus. Living specimens were collected from 22 sampling locations ranging from Shetland to Portugal to determine the distribution of Ammonia genetic types across the NE Atlantic shelf biomes. We successfully imaged (via scanning electron microscopy, SEM) and genotyped 378 Ammonia specimens, based on the small subunit (SSU) rRNA gene, linking morphology to genetic type. Phylogenetic analyses enabled identification of seven genetic types and subtypes inhabiting the NE Atlantic margins. Where possible, we linked SSU genetic types to the established large subunit (LSU) T-type nomenclature of Hayward et al. (2004). SSU genetic types with no matching T-type LSU gene sequences in GenBank were allocated new T-numbers to bring them in line with the widely adopted T-type nomenclature. The genetic types identified in the NE Atlantic margins are T1, T2, T3, T6, and T15, with both T2 and T3 being split further into the subtypes T2A and T2B, and T3S and T3V respectively. The seven genetic types and subtypes exhibit different biogeographical distributions and/or ecological preferences, but co-occurrence of two or more genetic types is common. A shore-line transect at Dartmouth (South England) demonstrates that sampling position on shore (high, middle or low shore) influences the genetic type collected, the numbers of genetic types that co-occur, and the numbers of individuals collected. We performed morphometric analysis on the SEM images of 158 genotyped Ammonia specimens. T15 and the subtypes T3S and T3V can be morphologically distinguished. We can unequivocally assign the taxonomic names A. batava and A. falsobeccarii to T3S and T15, respectively. However, the end members of T1, T2A, T2B and T6 cannot be unambiguously distinguished, and therefore these genetic types are partially cryptic. However, we confirm that T2A can be assigned to A. aberdoveyensis, but caution must be taken in warm provinces where the presence of T2B will complicate the morphological identification of T2A. We suggest that T6 should not currently be allocated to the Pliocene species A. aomoriensis due to morphological discrepancies with the taxonomic description and to the lack of genetic information. Of significance is that these partially cryptic genetic types frequently co-occur, which has considerable implications for precise species identification and accurate data interpretation.
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| 3. |
- Choquel, Constance, et al.
(author)
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Denitrification by benthic foraminifera and their contribution to N-loss from a fjord environment
- 2021
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In: Biogeosciences. - : Copernicus GmbH. - 1726-4170 .- 1726-4189. ; 18:1, s. 327-341
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Journal article (peer-reviewed)abstract
- Oxygen and nitrate availabilities impact the marine nitrogen cycle at a range of spatial and temporal scales. Here, we demonstrate the impact of denitrifying foraminifera on the nitrogen cycle at two oxygen and nitrate contrasting stations in a fjord environment (Gullmar Fjord, Sweden). Denitrification by benthic foraminifera was determined through the combination of specific density counting per microhabitat and specific nitrate respiration rates obtained through incubation experiments using N2O microsensors. Benthic nitrate removal was calculated from submillimeter chemical gradients extracted from 2D porewater images of the porewater nitrate concentration. These were acquired by combining the DET technique (diffusive equilibrium in thin film) with chemical colorimetry and hyperspectral imagery. Sediments with high nitrate concentrations in the porewater and oxygenated overlying water were dominated by the non-indigenous species (NIS) Nonionella sp. T1. Denitrification by this species could account for 50 %-100 % of the nitrate loss estimated from the nitrate gradients. In contrast sediments below hypoxic bottom waters had low inventories of porewater nitrate, and denitrifying foraminifera were rare. Their contribution to benthic nitrate removal was negligible (< 5 %). Our study showed that benthic foraminifera can be a major contributor to nitrogen mitigation in oxic coastal ecosystems and should be included in ecological and diagenetic models aiming to understand biogeochemical cycles coupled to nitrogen.
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| 4. |
- Jauffrais, Thierry, et al.
(author)
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Kleptoplastidic benthic foraminifera from aphotic habitats : insights into assimilation of inorganic C, N and S studied with sub-cellular resolution
- 2019
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In: Environmental Microbiology. - : Wiley. - 1462-2912. ; 21:1, s. 125-141
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Journal article (peer-reviewed)abstract
- The assimilation of inorganic compounds in foraminiferal metabolism compared to predation or organic matter assimilation is unknown. Here, we investigate possible inorganic-compound assimilation in Nonionellina labradorica, a common kleptoplastidic benthic foraminifer from Arctic and North Atlantic sublittoral regions. The objectives were to identify the source of the foraminiferal kleptoplasts, assess their photosynthetic functionality in light and darkness and investigate inorganic nitrogen and sulfate assimilation. We used DNA barcoding of a ~ 830 bp fragment from the SSU rDNA to identify the kleptoplasts and correlated transmission electron microscopy and nanometre-scale secondary ion mass spectrometry (TEM-NanoSIMS) isotopic imaging to study 13C-bicarbonate, 15N-ammonium and 34S-sulfate uptake. In addition, respiration rate measurements were determined to assess the response of N. labradorica to light. The DNA sequences established that over 80% of the kleptoplasts belonged to Thalassiosira (with 96%–99% identity), a cosmopolitan planktonic diatom. TEM-NanoSIMS imaging revealed degraded cytoplasm and an absence of 13C assimilation in foraminifera exposed to light. Oxygen measurements showed higher respiration rates under light than dark conditions, and no O2 production was detected. These results indicate that the photosynthetic pathways in N. labradorica are not functional. Furthermore, N. labradorica assimilated both 15N-ammonium and 34S-sulfate into its cytoplasm, which suggests that foraminifera might have several ammonium or sulfate assimilation pathways, involving either the kleptoplasts or bona fide foraminiferal pathway(s) not yet identified.
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| 5. |
- LeKieffre, Charlotte, et al.
(author)
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Ammonium and Sulfate Assimilation Is Widespread in Benthic Foraminifera
- 2022
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In: Frontiers in Marine Science. - : Frontiers Media SA. - 2296-7745. ; 9
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Journal article (peer-reviewed)abstract
- Nitrogen and sulfur are key elements in the biogeochemical cycles of marine ecosystems to which benthic foraminifera contribute significantly. Yet, cell-specific assimilation of ammonium, nitrate and sulfate by these protists is poorly characterized and understood across their wide range of species-specific trophic strategies. For example, detailed knowledge about ammonium and sulfate assimilation pathways is lacking and although some benthic foraminifera are known to maintain intracellular pools of nitrate and/or to denitrify, the potential use of nitrate-derived nitrogen for anabolic processes has not been systematically studied. In the present study, NanoSIMS isotopic imaging correlated with transmission electron microscopy was used to trace the incorporation of isotopically labeled inorganic nitrogen (ammonium or nitrate) and sulfate into the biomass of twelve benthic foraminiferal species from different marine environments. On timescales of twenty hours, no detectable 15N-enrichments from nitrate assimilation were observed in species known to perform denitrification, indicating that, while denitrifying foraminifera store intra-cellular nitrate, they do not use nitrate-derived nitrogen to build their biomass. Assimilation of both ammonium and sulfate, with corresponding 15N and 34S-enrichments, were observed in all species investigated (with some individual exceptions for sulfate). Assimilation of ammonium and sulfate thus can be considered widespread among benthic foraminifera. These metabolic capacities may help to underpin the ability of benthic foraminifera to colonize highly diverse marine habitats.
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| 6. |
- LeKieffre, Charlotte, et al.
(author)
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An overview of cellular ultrastructure in benthic foraminifera : New observations of rotalid species in the context of existing literature
- 2018
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In: Marine Micropaleontology. - : Elsevier BV. - 0377-8398. ; 138, s. 12-32
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Journal article (peer-reviewed)abstract
- We report systematic transmission electron microscope (TEM) observations of the cellular ultrastructure of selected, small rotalid benthic foraminifera. Nine species from different environments (intertidal mudflat, fjord, and basin) were investigated: Ammonia sp., Elphidium oceanense, Haynesina germanica, Bulimina marginata, Globobulimina sp., Nonionellina labradorica, Nonionella sp., Stainforthia fusiformis and Buliminella tenuata. All the observed specimens were fixed just after collection from their natural habitats allowing description of intact and healthy cells. Foraminiferal organelles can be divided into two broad categories: (1) organelles that are present in all eukaryotes, such as the nuclei, mitochondria, endoplasmic reticulum, Golgi apparatus, and peroxisomes; and (2) organelles observed in all foraminifera but not common in all eukaryotic cells, generally with unknown function, such as fibrillar vesicles or electron-opaque bodies. Although the organelles of the first category were observed in all the observed species, their appearance varies. For example, subcellular compartments linked to feeding and metabolism exhibited different sizes and shapes between species, likely due to differences in their diet and/or trophic mechanisms. The organelles of the second category are common in all foraminiferal species investigated and, according to the literature, are frequently present in the cytoplasm of many different species, both benthic and planktonic. This study, thus, provides a detailed overview of the major ultrastructural components in benthic foraminiferal cells from a variety of marine environments, and also highlights the need for further research to better understand the function and role of the various organelles in these fascinating organisms.
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| 7. |
- Polovodova Asteman, Irina, 1980, et al.
(author)
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Distribution of the putative invasive species Nonionella sp. T1 in the Gullmar Fjord – What is its potential contribution to biogeochemical cycles?
- 2023
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In: International Congress FORAMS2023, Perugia, Italy 25-30th June 2023.
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Conference paper (other academic/artistic)abstract
- Benthic foraminifera, both fossil and living, have been extensively studied in the seasonally hypoxic Gullmar Fjord (Sweden) for decades to decipher hydrographic changes and ecological status. In 2011, a non-indigenous species named Nonionella sp. T1 was discovered in the fjord for the first time. Here, we aim at evaluating its putative invasive behavior and life strategies by combining assemblage analyses of living foraminifera along a fjord transect of surface sediment (0-3 cm) together with four longer sediment cores (0-5 cm) from two stations at 51 m and 117 m water depth. Our results showed that Nonionella sp. T1 collected in the surface sediment in September 2021 and 2022, was present in almost all the transect samples. This species dominated the living foraminiferal assemblages with an abundance between 15 and 72 %, at seven of the eight sites visited. The highest relative and absolute abundances were noted between 39 and 78 m water depth, proximal to the fjord mouth, with a reduced presence towards the deepest station and the fjord head. However, Nonionella sp. T1 was completely absent in the sandy sediments at the shallowest station (1 m water depth). Sediment cores collected in November 2017 and May 2022 revealed that Nonionella sp. T1 exhibited higher abundance at 51 m water depth compared to 117 m. In a previous study, higher densities were observed at the station 51 m below the oxygenated sediment zone (< 2 mm depth), where high nitrate concentrations in pore waters were measured (2017 data). The authors demonstrated that Nonionella sp. T1 respires nitrate and the pool of specimens denitrifies up to 50 % – 100 % of the nitrate in sediment porewaters, revealing its non-negligible contribution to benthic denitrification. The 10-fold higher abundance of Nonionella sp. T1 recorded in 2022 (compared to 2017) supports previous hypotheses about their invasive character and alerts about their important role in the nitrogen cycle of the Gullmar Fjord. The results of this study highlight the need for continued monitoring of this invasive species, its spreading dynamics and ecological/biogeochemical impacts.
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| 8. |
- Schweizer, Magali, et al.
(author)
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Trophic strategies of intertidal foraminifera explored with single-cell microbiome metabarcoding and morphological methods : What is on the menu?
- 2022
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In: Ecology and Evolution. - : Wiley. - 2045-7758. ; 12:11
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Journal article (peer-reviewed)abstract
- In mudflats, interactions and transfers of nutrients and secondary metabolites may drive ecosystems and biodiversity. Foraminifera have complex trophic strategies as they often rely on bacteria and eukaryotes or on potential symbionts for carbon and nitrogen resources. The capacity of these protists to use a wide range of adaptive mechanisms requires clarifying the relationships between them and their microbial associates. Here, we investigate the interactions of three foraminiferal species with nearby organisms in situ, by coupling molecular (cloning/Sanger and high-throughput sequencing) and direct counting and morphological identification with microscopy. This coupling allows the identification of the organisms found in or around three foraminiferal species through molecular tools combined with a direct counting of foraminifera and diatoms present in situ through microscopy methods. Depending on foraminiferal species, and in addition to diatom biomass, diatom frustule shape, size and species are key factors driving the abundance and diversity of foraminifera in mudflat habitats. Three different trophic strategies were deduced for the foraminifera investigated in this study: Ammonia sp. T6 has an opportunistic strategy and is feeding on bacteria, nematoda, fungi, and diatoms when abundant; Elphidium oceanense is feeding mainly on diatoms, mixed with other preys when they are less abundant; and Haynesina germanica is feeding almost solely on medium-large pennate diatoms. Although there are limitations due to the lack of species coverage in DNA sequence databases and to the difficulty to compare morphological and molecular data, this study highlights the relevance of combining molecular with morphological tools to study trophic interactions and microbiome communities of protists at the single-cell scale.
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