A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

Gibbin, Emma M.; Banc-Prandi, Guilhem; Fine, Maoz; Comment, Arnaud; Meibom, Anders

doi:10.1038/s42003-019-0742-6

Cited by 9 publications

(11 citation statements)

References 26 publications

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“…proteins, fatty acids, RNA, DNA, etc. representing the products of anabolic metabolism, remain [ 41 , 42 ]. Isotopic enrichments shown in the following thus represent the relative anabolic turnover of the tissue during the incubation experiments.…”

Section: Resultsmentioning

confidence: 99%

Amoebocytes facilitate efficient carbon and nitrogen assimilation in theCassiopea-Symbiodiniaceae symbiosis

et al. 2020

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The upside-down jellyfish Cassiopea engages in symbiosis with photosynthetic microalgae that facilitate uptake and recycling of inorganic nutrients. By contrast to most other symbiotic cnidarians, algal endosymbionts in Cassiopea are not restricted to the gastroderm but are found in amoebocyte cells within the mesoglea. While symbiont-bearing amoebocytes are highly abundant, their role in nutrient uptake and cycling in Cassiopea remains unknown. By combining isotopic labelling experiments with correlated scanning electron microscopy, and Nano-scale secondary ion mass spectrometry (NanoSIMS) imaging, we quantified the anabolic assimilation of inorganic carbon and nitrogen at the subcellular level in juvenile Cassiopea medusae bell tissue. Amoebocytes were clustered near the sub-umbrella epidermis and facilitated efficient assimilation of inorganic nutrients. Photosynthetically fixed carbon was efficiently translocated between endosymbionts, amoebocytes and host epidermis at rates similar to or exceeding those observed in corals. The Cassiopea holobionts efficiently assimilated ammonium, while no nitrate assimilation was detected, possibly reflecting adaptation to highly dynamic environmental conditions of their natural habitat. The motile amoebocytes allow Cassiopea medusae to distribute their endosymbiont population to optimize access to light and nutrients, and transport nutrition between tissue areas. Amoebocytes thus play a vital role for the assimilation and translocation of nutrients in Cassiopea , providing an interesting new model for studies of metabolic interactions in photosymbiotic marine organisms.

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Section: Resultsmentioning

confidence: 99%

Amoebocytes facilitate efficient carbon and nitrogen assimilation in theCassiopea-Symbiodiniaceae symbiosis

et al. 2020

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“…Note that TEM-NanoSIMS sample preparation leads to the loss of all soluble compounds. Therefore, only 13 C and 15 N assimilated in the biomass can be measured ( Nomaki et al, 2018 ; Gibbin et al, 2020 ; Loussert-Fonta et al, 2020 ). T -tests were performed to verify whether there was a significant difference in the δ 15 N and δ 13 C of different cellular compartments of Ammonia sp.…”

Section: Methodsmentioning

confidence: 99%

Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

et al. 2020

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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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“…Their ecological success in nutrient-poor tropical waters is due to the sharing and the tight recycling of nutrients between the partners [5,6]. Symbionts, through photosynthesis, transform dissolved inorganic carbon (DIC) and nitrogen (DIN), as well as other nutrients, into organic molecules which are translocated to the host for most of its metabolic needs, such as respiration, calcification and energetic reserves [7][8][9]. In turn, the animal provides its symbionts with nutrients coming from the environment and from its metabolic waste products [10][11][12].…”

Section: Introductionmentioning

confidence: 99%

“…An efficient acquisition of DIC by the symbionts is a key process for the health of the symbiotic association, because the amount of DIC fixed and assimilated by the symbionts will also determine the amount of photosynthates transferred to the host for its own needs [9]. Both partners have developed multiple ways of acquiring and concentrating carbon for photosynthesis.…”

Section: Introductionmentioning

confidence: 99%

Coral Productivity Is Co-Limited by Bicarbonate and Ammonium Availability

et al. 2020

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The nitrogen environment and nitrogen status of reef-building coral endosymbionts is one of the important factors determining the optimal assimilation of phototrophic carbon and hence the growth of the holobiont. However, the impact of inorganic nutrient availability on the photosynthesis and physiological state of the coral holobiont is partly understood. This study aimed to determine if photosynthesis of the endosymbionts associated with the coral Stylophora pistillata and the overall growth of the holobiont were limited by the availability of dissolved inorganic carbon and nitrogen in seawater. For this purpose, colonies were incubated in absence or presence of 4 µM ammonium and/or 6 mM bicarbonate. Photosynthetic performances, pigments content, endosymbionts density and growth rate of the coral colonies were monitored for 3 weeks. Positive effects were observed on coral physiology with the supplementation of one or the other nutrient, but the most important changes were observed when both nutrients were provided. The increased availability of DIC and NH4+ significantly improved the photosynthetic efficiency and capacity of endosymbionts, in turn enhancing the host calcification rate. Overall, these results suggest that in hospite symbionts are co-limited by nitrogen and carbon availability for an optimal photosynthesis.

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A method to disentangle and quantify host anabolic turnover in photosymbiotic holobionts with subcellular resolution

Cited by 9 publications

References 26 publications

Amoebocytes facilitate efficient carbon and nitrogen assimilation in theCassiopea-Symbiodiniaceae symbiosis

Amoebocytes facilitate efficient carbon and nitrogen assimilation in theCassiopea-Symbiodiniaceae symbiosis

Heterotrophic Foraminifera Capable of Inorganic Nitrogen Assimilation

Coral Productivity Is Co-Limited by Bicarbonate and Ammonium Availability

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