Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

Lekieffre, Charlotte Madeleine Nicole; Spero, Howard J.; Russell, A. D.; Fehrenbacher, Jennifer S.; Geslin, Emmanuelle; Meibom, Anders

doi:10.1007/s00227-018-3362-7

Cited by 26 publications

(64 citation statements)

References 58 publications

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“…In this diagram, the necessity of photosymbiosis, i.e., whether the relationship is essential for the host survival, is not considered since we cannot go into a detailed interactional relationship with our method. A recent study using a 13 C pulsechase experiment of O. universa, subsequent subcellular microimaging, and elemental analysis revealed the fate of assimilated carbon by the symbionts (LeKieffre et al, 2018). They showed a line of evidence of substance transfer from the symbionts to the host and their tight interrelationship.…”

Section: Characteristics and A New Framework Of Planktonic Foraminifementioning

confidence: 99%

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Characterizing photosymbiosis in modern planktonic foraminifera

Takagi¹,

Kimoto²,

Fujiki³

et al. 2019

Biogeosciences

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Abstract. Photosymbiosis has played a key role in the diversification of foraminifera and their carbonate production throughout geologic history. However, identification of photosymbiosis in extinct taxa remains challenging, and even among the extant species the occurrence and functional relevance of photosymbiosis remain poorly constrained. Here, we investigate photosymbiosis in living planktonic foraminifera by measuring active chlorophyll fluorescence with fast repetition rate fluorometry. This method provides unequivocal evidence for the presence of photosynthetic capacity in individual foraminifera, and it allows us to characterize multiple features of symbiont photosynthesis including chlorophyll a (Chl a) content, potential photosynthetic activity (Fv∕Fm), and light-absorption efficiency (σPSII). To obtain robust evidence for the occurrence and importance of photosymbiosis in modern planktonic foraminifera, we conducted measurements on 1266 individuals from 30 species of the families Globigerinidae, Hastigerinidae, Globorotaliidae, and Candeinidae. Among the studied species, 19 were recognized as symbiotic and 11 as non-symbiotic. Of these, six species were newly confirmed as symbiotic and five as non-symbiotic. Photosymbiotic species have been identified in all families except the Hastigerinidae. A significant positive correlation between test size and Chl a content, found in 16 species, is interpreted as symbiont abundance scaled to the growth of the host and is consistent with persistent possession of symbionts through the lifetime of the foraminifera. The remaining three symbiont-bearing species did not show such a relationship, and their Fv∕Fm values were comparatively low, indicating that their symbionts do not grow once acquired from the environment. The objectively quantified photosymbiotic characteristics have been used to design a metric of photosymbiosis, which allows the studied species to be classified along a gradient of photosynthetic activity, providing a framework for future ecological and physiological investigations of planktonic foraminifera.

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Section: Characteristics and A New Framework Of Planktonic Foraminifementioning

confidence: 99%

“…Globigerinella siphonifera was divided Table S1 for detailed sampling information. Annual sea surface temperature (SST) data were from the World Ocean Atlas 2013 (Locarnini et al, 2013).…”

Section: Sampling and Identification Of Morphological Speciesmentioning

confidence: 99%

Characterizing photosymbiosis in modern planktonic foraminifera

Takagi¹,

Kimoto²,

Fujiki³

et al. 2019

Biogeosciences

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“…In return for metabolic ammonium and phosphate from the host, these symbionts photosynthesize and transfer a portion of the resulting organic matter to the foraminifer (Uhle et al, 1999), supplementing the organic carbon that it obtains from its largely carnivorous diet (Anderson et al, 1979;Spindler et al, 1984). These dinoflagellate-bearing foraminifera appear to depend on their photosymbionts for survival (i.e., "obligatory" symbiosis; Hemleben et al, 1989), such that they are functionally mixotrophic rather than heterotrophic (Le Kieffre et al, 2018;Stoecker et al, 2009;Stoecker et al, 2017). Some of these (sub)tropical foraminifer species (e.g., O. universa) also occur in the Subantarctic Zone (SAZ; between the Subantarctic Front, SAF, and the Subtropical Front, STF; King & Howard, 2003;Mortyn & Charles, 2003).…”

Section: Introductionmentioning

confidence: 99%

The Nitrogen Isotopic Composition of Tissue and Shell‐Bound Organic Matter of Planktic Foraminifera in Southern Ocean Surface Waters

Smart

Fawcett

Ren

et al. 2020

Geochem Geophys Geosyst

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We present the first nitrogen isotope (δ15N) measurements of planktic foraminifera, paleoceanographically important zooplankton, from the nutrient‐rich waters of the modern Southern Ocean. Foraminifera were collected from net tows in the Subantarctic and Polar Frontal Zones (SAZ and PFZ, respectively) south of Africa during winter 2015 and late summer 2016. In late summer, consistent with preferential uptake of 14N‐nitrate and the progressive, northward depletion of nitrate by phytoplankton across the Southern Ocean, foraminifer tissue and shell‐bound δ15N rise equatorward along with nitrate δ15N. However, foraminifer δ15N is ~3‰ lower than expected for heterotrophs relying on photosynthetic biomass generated directly from nitrate. This discrepancy appears to originate with the particulate organic N (PON) in late‐summer surface waters, the δ15N of which is lowered by ammonium recycling. In winter, when overall productivity and foraminifer production are reduced, foraminifer δ15N is higher (by 4.6 ± 0.8‰ for tissue and by 4.0 ± 1.5‰ for shell‐bound N compared to late summer) and exhibits no clear north‐south trend. These characteristics can also be explained by the feeding‐driven connection of foraminifera to PON, which is elevated in δ15N by net degradation in winter. Therefore, foraminifer δ15N is more closely tied to PON δ15N than to nitrate δ15N in the Southern Ocean mixed layer. Combining our isotope data with previously reported sediment trap fluxes from the western Pacific SAZ/PFZ suggests that, under modern conditions, the late‐summer ammonium recycling signal outweighs that of wintertime decomposition on the annually integrated δ15N of sinking foraminifera.

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“…NH þ 4 or NO 2À 3 ) is scarce and often limits biological productivity [4]. Bulk δ 15 N data from cultured foraminifera, measured after 15 N-spiked experiments, showed N-compound translocation from the endosymbionts to the foraminifera host cell [5]. When nitrate is not limiting in the environment, model calculations revealed that up to 57% of the foraminiferal N could be translocated from the symbionts, and even up to 90-100% for model calculations taking into account nitrogen uptake by the symbionts from the recycled ammonium pool.…”

Section: Introductionmentioning

confidence: 99%

Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts

et al. 2020

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The symbiotic planktonic foraminifera Orbulina universa inhabits open ocean oligotrophic ecosystems where dissolved nutrients are scarce and often limit biological productivity. It has previously been proposed that O. universa meets its nitrogen (N) requirements by preying on zooplankton, and that its symbiotic dinoflagellates recycle metabolic ‘waste ammonium’ for their N pool. However, these conclusions were derived from bulk 15 N-enrichment experiments and model calculations, and our understanding of N assimilation and exchange between the foraminifer host cell and its symbiotic dinoflagellates remains poorly constrained. Here, we present data from pulse-chase experiments with 13 C-enriched inorganic carbon, 15 N-nitrate, and 15 N-ammonium, as well as a 13 C- and 15 N- enriched heterotrophic food source, followed by TEM (transmission electron microscopy) coupled to NanoSIMS (nanoscale secondary ion mass spectrometry) isotopic imaging to visualize and quantify C and N assimilation and translocation in the symbiotic system. High levels of 15 N-labelling were observed in the dinoflagellates and in foraminiferal organelles and cytoplasm after incubation with 15 N-ammonium, indicating efficient ammonium assimilation. Only weak 15 N-assimilation was observed after incubation with 15 N-nitrate. Feeding foraminifers with 13 C- and 15 N-labelled food resulted in dinoflagellates that were labelled with 15 N, thereby confirming the transfer of 15 N-compounds from the digestive vacuoles of the foraminifer to the symbiotic dinoflagellates, likely through recycling of ammonium. These observations are important for N isotope-based palaeoceanographic reconstructions, as they show that δ 15 N values recorded in the organic matrix in symbiotic species likely reflect ammonium recycling rather than alternative N sources, such as nitrates.

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Assimilation, translocation, and utilization of carbon between photosynthetic symbiotic dinoflagellates and their planktic foraminifera host

Cited by 26 publications

References 58 publications

Characterizing photosymbiosis in modern planktonic foraminifera

Characterizing photosymbiosis in modern planktonic foraminifera

The Nitrogen Isotopic Composition of Tissue and Shell‐Bound Organic Matter of Planktic Foraminifera in Southern Ocean Surface Waters

Ammonium is the preferred source of nitrogen for planktonic foraminifer and their dinoflagellate symbionts

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