Response of a kleptoplastidic foraminifer to heterotrophic starvation: photosynthesis and lipid droplet biogenesis

Jauffrais, Thierry; Lekieffre, Charlotte Madeleine Nicole; Schweizer, Magali; Jesus, Bruno; Metzger, Édouard; Geslin, Emmanuelle

doi:10.1093/femsec/fiz046

Cited by 12 publications

(22 citation statements)

References 73 publications

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“…In addition, the Nephroselmis 18S rRNA sequence was placed with a representative selection of Nephroselmis spp. sequences taken from GenBank (similarly to [ 102 , 103 ] with diatoms). The microalgal 18SrRNA sequence was deposited in GenBank (GenBank accession number: MT833289).…”

Section: Methodsmentioning

confidence: 99%

Effects of Nitrogen Availability on the Antioxidant Activity and Carotenoid Content of the Microalgae Nephroselmis sp

Coulombier¹,

Nicolau

Déan

et al. 2020

Marine Drugs

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Nephroselmis sp. was previously identified as a species of interest for its antioxidant properties owing to its high carotenoid content. In addition, nitrogen availability can impact biomass and specific metabolites’ production of microalgae. To optimize parameters of antioxidant production, Nephroselmis sp. was cultivated in batch and continuous culture conditions in stirred closed photobioreactors under different nitrogen conditions (N-repletion, N-limitation, and N-starvation). The aim was to determine the influence of nitrogen availability on the peroxyl radical scavenging activity (oxygen radical absorbance capacity (ORAC) assay) and carotenoid content of Nephroselmis sp. Pigment analysis revealed a specific and unusual photosynthetic system with siphonaxanthin-type light harvesting complexes found in primitive green algae, but also high lutein content and xanthophyll cycle pigments (i.e., violaxanthin, antheraxanthin, and zeaxanthin), as observed in most advanced chlorophytes. The results indicated that N-replete conditions enhance carotenoid biosynthesis, which would correspond to a higher antioxidant capacity measured in Nephroselmis sp. Indeed, peroxyl radical scavenging activity and total carotenoids were higher under N-replete conditions and decreased sharply under N-limitation or starvation conditions. Considering individual carotenoids, siphonaxanthin, neoxanthin, xanthophyll cycle pigments, and lycopene followed the same trend as total carotenoids, while β-carotene and lutein stayed stable regardless of the nitrogen availability. Carotenoid productivities were also higher under N-replete treatment. The peroxyl radical scavenging activity measured with ORAC assay (63.6 to 154.9 µmol TE g−1 DW) and the lutein content (5.22 to 7.97 mg g−1 DW) were within the upper ranges of values reported previously for other microalgae. Furthermore, contents of siphonaxanthin ere 6 to 20% higher than in previous identified sources (siphonous green algae). These results highlight the potential of Nephroselmis sp. as a source of natural antioxidant and as a pigment of interest.

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Section: Methodsmentioning

confidence: 99%

Effects of Nitrogen Availability on the Antioxidant Activity and Carotenoid Content of the Microalgae Nephroselmis sp

Coulombier¹,

Nicolau

Déan

et al. 2020

Marine Drugs

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“…Some benthic foraminifera are capable of sequestering chloroplasts from their microalgal food source, i.e. diatoms [ 5 , 14 – 16 ] and retain them photosynthetically active in their cytosol [ 15 , 17 – 19 ]. This process of sequestering and exploiting foreign plastids is referred to as kleptoplastidy [ 20 ] and has been extensively studied in sacoglossan gastropods e.g.…”

Section: Introductionmentioning

confidence: 99%

“…Presently, only four kleptoplastidic foraminifer species (all found on intertidal mudflats) have been described as photosynthetically active, i.e. Haynesina germanica , Elphidium crispum , Elphidium williamsoni and Planoglabratella opercularis [ 8 , 14 , 17 – 19 , 34 , 40 ], while the functionality of the xanthophyll cycle photo-regulation mechanism has only been studied in H. germanica [ 42 ].…”

Section: Introductionmentioning

confidence: 99%

“…In the present study, we investigate relationships between feeding strategies, kleptoplast spatial distribution and photosynthetic functionality in two shallow-water benthic foraminifera ( H. germanica and E. williamsoni ) exhibiting different kleptoplast retention-times and different levels of functionality [ 14 , 18 ]. This was achieved by coupling—for the first time—observations of foraminiferal feeding behaviour, test morphology, cytological TEM-based observations and HPLC pigment analysis, with non-destructive, single-cell level imaging of kleptoplast spatial distribution and kleptoplast photosystem II (PSII) quantum efficiency in live foraminifera.…”

Section: Introductionmentioning

confidence: 99%

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Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera

et al. 2021

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Foraminifera are ubiquitously distributed in marine habitats, playing a major role in marine sediment carbon sequestration and the nitrogen cycle. They exhibit a wide diversity of feeding and behavioural strategies (heterotrophy, autotrophy and mixotrophy), including species with the ability of sequestering intact functional chloroplasts from their microalgal food source (kleptoplastidy), resulting in a mixotrophic lifestyle. The mechanisms by which kleptoplasts are integrated and kept functional inside foraminiferal cytosol are poorly known. In our study, we investigated relationships between feeding strategies, kleptoplast spatial distribution and photosynthetic functionality in two shallow-water benthic foraminifera (Haynesina germanica and Elphidium williamsoni), both species feeding on benthic diatoms. We used a combination of observations of foraminiferal feeding behaviour, test morphology, cytological TEM-based observations and HPLC pigment analysis, with non-destructive, single-cell level imaging of kleptoplast spatial distribution and PSII quantum efficiency. The two species showed different feeding strategies, with H. germanica removing diatom content at the foraminifer’s apertural region and E. williamsoni on the dorsal site. All E. williamsoni parameters showed that this species has higher autotrophic capacity albeit both feeding on benthic diatoms. This might represent two different stages in the evolutionary process of establishing a permanent symbiotic relationship, or may reflect different trophic strategies.

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“…SEM images of N. labradorica's aperture show a specific ornamentation, possibly a morphological adaptation to this "predatory" mode of life for obtaining the kleptoplasts (Bernhard and Bowser, 1999). It is speculated that in deep-sea specimens the function of kleptoplasts is rather related to the sulfur cycle rather than with photosynthesis (Jauffrais et al, 2019). Our study does not concentrate on kleptoplasts but rather analyzed feeding preferences and contents of the degradation vacuoles of this species from an active methane-emitting site in the Arctic (Storfjordrenna, Barents Sea).…”

Section: Introductionmentioning

confidence: 99%

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

Schmidt

Geslin²,

Bernhard

et al. 2021

Preprint

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Abstract. Several foraminifera are deposit feeders that consume organic detritus (dead particulate organic material along with entrained bacteria). However, the role of such foraminifera in the benthic food-web remains understudied. As foraminifera may associate with methanotrophic bacteria, which are 13C-depleted, feeding on them has been suggested to cause negative δ13C values in the foraminiferal cytoplasm and/or calcite. To test whether the foraminiferal diet includes methanotrophs, we performed a short-term (1 d) feeding experiment with Nonionellina labradorica from an active Arctic methane-emission site (Storfjordrenna, Barents Sea) using the marine methanotroph Methyloprofundus sedimenti, and analyzed N. labradorica cytology via Transmission Electron microscopy (TEM). We hypothesized that M. sedimenti would be visible, as evidenced by their ultrastructure, in degradation vacuoles after this feeding experiment. Sediment grains (mostly clay) occurred inside one or several degradation vacuoles in all foraminifers. In 24 % of the specimens from the feeding experiment degradation vacuoles also contained bacteria, although none could be confirmed to be the offered M. sedimenti. Observations of the area adjacent to the aperture after 20 h incubation revealed three putative methanotrophs, close to clay particles. These methanotrophs were identified based on internal characteristics such as a type I stacked intracytoplasmic membranes (ICM), storage granules (SG) and gram-negative cell walls (GNCW). Furthermore, N. labradorica specimens were examined for specific adaptations to this active Arctic methane-emission site; we noted the absence of bacterial endobionts in all specimens examined but confirmed the presence of kleptoplasts, which were often partially degraded. Based on these observations, we suggest that M. sedimenti can be consumed by N. labradorica via untargeted grazing in seeps and that N. labradorica can be generally classified as a deposit feeder at this Arctic site. These results suggest that if methanothrophs are available to the foraminifera in their habitat, their non-selective uptake could make a substantial contribution to altering δ13Ctest values. This in turn may impact metazoans grazing on benthic foraminifera by altering their δ13C signature.

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Response of a kleptoplastidic foraminifer to heterotrophic starvation: photosynthesis and lipid droplet biogenesis

Abstract: Please note that this is an author-produced PDF of an article accepted for publication following peer review. The definitive publisher-authenticated version is available on the publisher Web site.

Cited by 12 publications

References 73 publications

Effects of Nitrogen Availability on the Antioxidant Activity and Carotenoid Content of the Microalgae Nephroselmis sp

Effects of Nitrogen Availability on the Antioxidant Activity and Carotenoid Content of the Microalgae Nephroselmis sp

Kleptoplast distribution, photosynthetic efficiency and sequestration mechanisms in intertidal benthic foraminifera

Deposit feeding of a foraminifera from an Arctic methane seep site and possible association with a methanotroph revealed by transmission electron microscopy

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