Ammonium enhancement of dark carbon fixation and nitrogen limitation in symbiotic zooxanthellae: Effects of feeding and starvation of the sea anemone Aiptasia pallida

Cook, Clayton B.; Muller‐Parker, Gisèle; D’Elia, Christopher F.

doi:10.4319/lo.1992.37.1.0131

Cited by 49 publications

(35 citation statements)

References 14 publications

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“…This cycle indeed shows that, in starved corals, uptake rates measured over 12 h (daylight period) were comparable to those measured over 24 h (day and night incubation). This suggests that uptake by these animals and in our conditions was constant throughout the 24 h. Ammonium uptake in the dark has been demonstrated by a number of other studies (Muscatine and D'Elia 1978;Wilkerson and Trench 1986) and has been suggested to increase the rate at which carbon is fixed by the zooxanthellae in darkness (Cook et al 1992). However, in fed corals, uptake rates were four times lower when measured for 24 than 12 h. Two hypotheses might explain such a difference: (1) zooxanthellae stopped taking up ammonium during the dark period, and/or (2) well-fed animals might have excreted nitrogen during the night.…”

Section: Discussionsupporting

confidence: 73%

Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations

Grover

Maguer

Reynaud-Vaganay

et al. 2002

Limnology & Oceanography

168

167

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Experiments were designed to assess the uptake rates of 0.2, 1, and 5 M ammonium by the scleractinian coral Stylophora pistillata maintained under different feeding regimes (highly fed, slightly fed, and starved) for 4-8 weeks.15 NH 4 was used to follow the incorporation of nitrogen in the zooxanthellae or in the animal tissue and to calculate uptake rates. After 4 or 8 weeks, fed corals contained significantly higher concentrations of protein, chlorophyll, and zooxanthellae than starved nubbins. They also contained significantly higher amounts of carbon and nitrogen per unit surface skeleton. Results obtained showed that the algal fraction was enriched with 15 N at up to 10 times the rate of the host, which suggests that the zooxanthellae are the primary site of assimilation. Uptake rates (measured in the algal fraction) varied according to the nitrogen concentration in seawater. They were ϳ20 times lower at 0.2 than at 1 or 5 M 15 NH 4 enrichment (2-30 vs. 120-510 ng N h Ϫ1 cm Ϫ2 ) for both fed and starved nubbins. These rates were also affected by the feeding history of the host, because they were significantly lower for fed than for starved nubbins (analysis of variance, P Ͻ 0.005), at both high and low ammonium concentrations. On the basis of the nitrogen content of the zooxanthellae, we suggest that an external concentration of ammonium equal to 0.6 M can sustain the growth of the zooxanthellae population.

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Section: Discussionsupporting

confidence: 73%

Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations

Grover

Maguer

Reynaud-Vaganay

et al. 2002

Limnology & Oceanography

168

167

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“…Symbiotic sea anemones, like other symbiotic cnidarians, still need to feed. In fact, cessation of feeding by Aiptasia pallida was correlated with nutrient deficiency in the zooxanthellae (Cook et al 1988(Cook et al , 1992. Periodical meals are therefore a necessity for the symbiosis to remain healthy.…”

Section: Discussionmentioning

confidence: 99%

Toxicological response of the symbiotic sea anemone Aiptasia pallida to butyltin contamination

Mercier¹,

Pelletier²,

Jf³

1996

Mar. Ecol. Prog. Ser.

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This study investigates the fate of tributyltin (TBT), a widespread biocide mainly used in antifouling paints, and of its derivative dibutyltin (DBT) in sea anemones Aiptasia pallida exposed via water or food. Experiments were conducted on both symbiotic and aposymbiotic (lacking zooxanthellae) individuals under a 12 h light: 12 h dark photoperiod or in total darkness. TBT and DBT concentrations in the animal and vegetal compartments were measured over 24 h, 30 h, 5 d. 7 d and 28 d periods. Uptake and accumulation from seawater, mainly as DBT due to natural degradation of TBT, was found to be dependent on the presence and illumination of zooxanthellae. DBT concentratlons in symbiotic anemones exposed to light were roughly twlce those found in individuals maintained ~n total darkness, and about 10 times greater than in aposymbiotic anemones. A peak accumulation in animal and vegetal tissues occurred after 24 to 4 8 h in all symbiotic anemones. A 28 d exposure of symbiotic anemones to a nominal 50 ng TBT 1-' resulted in butyltin concentrations under 1 ng mg-' dry mass. Accumulation most probably occurs through butyltln uptake by zooxanthellae, while their expulsion from the host acts as a depuration process. The presence of zooxanthellae also seems determinant in the regulation and degradation of butyltin ingested with food. Daily ingestion of TBT-contaminated mussel tissue led to sequential debutylation into DBT and monobutyltin (MBT) in symbiotic A . pallida but not in aposymbiotic ones. Over 7 d. aposymbiotic anemones showed close to 100% retention of ingested TBT, while all butyltin species remained undetected in symbiotic anemones. After 28 d, the retention efficiency was -68% in symbiotic anemones in which -59% of the butyltin was in the form of DBT

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“…Nitrogen acquisition and exchange are of great importance to corals due to the nutrient-poor water in which they exist (Cook et al, 1992;Grover et al, 2008;Rädecker et al, 2015), and symbiosis has been proposed to increase the efficiency of nitrogen utilization by both partners (Wang and Douglas, 1998). We detected an ammonium transporter in symbiotic Aiptasia that was not detected in aposymbiotic anemones (Table 2), supporting the role of symbiosis in nitrogen exchange.…”

Section: Nitrogen Metabolismmentioning

confidence: 99%

Symbiosis induces widespread changes in the proteome of the model cnidarianAiptasia

Oakley

Ameismeier²,

Peng

et al. 2016

Cellular Microbiology

103

138

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Coral reef ecosystems are metabolically founded on the mutualism between corals and photosynthetic dinoflagellates of the genus Symbiodinium. The glass anemone Aiptasia sp. has become a tractable model for this symbiosis, and recent advances in genetic information have enabled the use of mass spectrometry-based proteomics in this model. We utilized label-free liquid chromatography electrospray-ionization tandem mass spectrometry to analyze the effects of symbiosis on the proteomes of symbiotic and aposymbiotic Aiptasia. We identified and obtained relative quantification of more than 3,300 proteins in 1,578 protein clusters, with 81 protein clusters showing significantly different expression between symbiotic states. Symbiotic anemones showed significantly higher expression of proteins involved in lipid storage and transport, nitrogen transport and cycling, intracellular trafficking, endocytosis and inorganic carbon transport. These changes reflect shifts in host metabolism and nutrient reserves due to increased nutritional exchange with the symbionts, as well as mechanisms for supplying inorganic nutrients to the algae. Aposymbiotic anemones exhibited increased expression of multiple systems responsible for mediating reactive oxygen stress, suggesting that the host derives direct or indirect protection from oxidative stress while in symbiosis. Aposymbiotic anemones also increased their expression of an array of proteases and chitinases, indicating a metabolic shift from autotrophy to heterotrophy. These results provide a comprehensive Aiptasia proteome with more direct relative quantification of protein abundance than transcriptomic methods. The extension of "omics" techniques to this model system will allow more powerful studies of coral physiology, ecosystem function, and the effects of biotic and abiotic stress on the coral-dinoflagellate mutualism.

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Ammonium enhancement of dark carbon fixation and nitrogen limitation in symbiotic zooxanthellae: Effects of feeding and starvation of the sea anemone Aiptasia pallida

Cited by 49 publications

References 14 publications

Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations

Uptake of ammonium by the scleractinian coral Stylophora pistillata: Effect of feeding, light, and ammonium concentrations

Toxicological response of the symbiotic sea anemone Aiptasia pallida to butyltin contamination

Symbiosis induces widespread changes in the proteome of the model cnidarianAiptasia

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