Primary site and initial products of ammonium assimilation in the symbiotic sea anemone Anemonia viridis

Roberts, J. Murray; Davies, Phil; Fixter, L. M.; Preston, Tom

doi:10.1007/s002270050620

Cited by 46 publications

(39 citation statements)

References 41 publications

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“…In that study, 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. This pattern has also been found in other zooxanthellar symbiosis when they have been investigated by use of a 15 N tracer (Wilkerson and Kremer 1992;Hawkins and Klumpp 1995;Roberts et al 1999). The presence of 15 N in animal tissue after incubation in 15 NH 4 -spiked seawater is consistent with both the diffusion-depletion hypothesis (D'Elia et al 1983) and the possibility that 15 N is held in regulatory pools being maintained and released by animal enzyme activity (Wang and Douglas 1998).…”

Section: Discussionsupporting

confidence: 67%

“…Few studies, however, have measured the uptake rates of ammonium and nitrate under different environmental conditions. Most of the works were performed with cultured or freshly isolated zooxanthellae (D'Elia et al 1983;Domotor and D'Elia 1984;McAuley and Smith 1995), and only one work determined the pathway of ammonium assimilation in the symbiotic sea anemone Anemonia viridis (Roberts et al 1999). However, nitrogen uptake rates by the coral-zooxanthellae association have still been poorly investigated (Muscatine and D'Elia 1978;Burris 1983;Wilkerson and Trench 1986;Bythell 1990;Hoegh-Guldberg and Williamson 1999).…”

Section: Acknowledgmentsmentioning

confidence: 99%

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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: 67%

Section: Acknowledgmentsmentioning

confidence: 99%

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

View full text Add to dashboard Cite

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“…Zooxanthellae assimilate NH + 4 via the glutamine synthetase/glutamine:2-oxoglutarate aminotransferase (GS/GOGAT) cycle (D'elia et al, 1983;Roberts et al, 1999Roberts et al, , 2001, while the coral host assimilates it via the action of GS and/or glutamate dehydrogenase (Miller and Yellowlees, 1989;Wang and Douglas, 1998;Yellowlees et al, 2008). However, it has been demonstrated that zooxanthellae account for most of the NH + 4 uptake with assimilation rates 14-23 times faster compared to the coral host (Pernice et al, 2012).…”

Section: Mechanisms Of Ddn Uptake and Transfer Among Compartments Of mentioning

confidence: 99%

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

2017

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Coral reefs are highly productive ecosystems thriving in nutrient-poor waters. Their productivity depends largely on the availability of nitrogen, the proximate limiting nutrient for primary production. In reefs, the major nitrogen pathways include regeneration, nitrification, ammonification and dinitrogen (N 2 ) fixation. N 2 fixation is performed by prokaryotes called "diazotrophs" that abound in coral rubbles, sandy bottoms, microbial mats, or seagrass meadows. Corals, which are the main reef builders, have developed a partnership with dinoflagellates which transform dissolved inorganic nitrogen into amino acids and protein, and with diazotrophs to gain diazotrophically-derived nitrogen (DDN). Pioneering studies found active diazotrophic cyanobacteria in the corals' mucus and/or tissue, and later high throughput sequencing efforts have described diverse communities of non-cyanobacterial diazotrophs associated with scleractinian corals. Yet, the metabolic processes behind these associations and how they benefit corals are currently not well understood. While genomic studies describe the diversity of diazotrophs and isotopic tracer experiments quantify N 2 fixation rates, combined advanced methods are needed to elucidate the mechanisms behind the transfer of DDN to the coral holobiont and whether these mechanisms change according to the identity of the diazotrophs or coral species. Here we review our current knowledge on N 2 fixation in corals: the diversity and localization of diazotrophs in the coral holobiont, the environmental factors controlling N 2 fixation, the fate of DDN within the coral symbiosis as well as its potential role in coral resilience. We finally summarize the unknowns: are the diversity, abundance and localization of diazotrophs within the holobiont species-and/or site-specific? Do they have an impact on DDN production? What are the metabolic mechanisms implicated? Do they change spatially, temporally or according to environmental factors? We encourage scientists to undertake research efforts to tackle these questions in order to shed light on nitrogen cycling in reef ecosystems and to understand if coral-associated N 2 fixation can improve coral's resilience in the face of climate change.

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“…The main ammonium assimilatory pathway in dinoflagellate is via the GS/GOGAT cycle (Summons and Osmond, 1981;Summons et al, 1986;Rahav et al, 1989;Roberts et al, 1999) in which GS first transfers ammonium to glutamate to produce glutamine and GOGAT then completes the cycle by catalysing the conversion of glutamine and 2-oxoglutarate to produce Glutamate (Falkowski et al, 1993;Roberts et al, 1999;Inokuchi et al, 2002). The abundance of Glutamine and Glutamate is therefore supposed to be a sensitive indicator of assimilation of nitrogen following uptake of ammonium by dinoflagellate (Flynn et al, 1994).…”

Section: Metabolic Fate Of Ammonium Assimilated By Dinoflagellate Symmentioning

confidence: 99%

“…Both the coral host and the algae possess the enzymatic machinery required to incorporate ammonium into their tissues. It has been proposed that the majority of ammonium is assimilated either by the dinoflagellate symbiont via the glutamine synthetase/ glutamine:2-oxoglutarate aminotransferase (GS/ GOGAT) cycle (D'Elia et al, 1983;Roberts et al, 1999Roberts et al, , 2001 or by the coral host via the action of GS and/or glutamate dehydrogenase (Figure 1c) (Miller and Yellowlees, 1989;Wang and Douglas, 1998;Yellowlees et al, 2008).…”

Section: Introductionmentioning

confidence: 99%

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

et al. 2012

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Assimilation of inorganic nitrogen from nutrient-poor tropical seas is an essential challenge for the endosymbiosis between reef-building corals and dinoflagellates. Despite the clear evidence that reef-building corals can use ammonium as inorganic nitrogen source, the dynamics and precise roles of host and symbionts in this fundamental process remain unclear. Here, we combine high spatial resolution ion microprobe imaging (NanoSIMS) and pulse-chase isotopic labeling in order to track the dynamics of ammonium incorporation within the intact symbiosis between the reefbuilding coral Acropora aspera and its dinoflagellate symbionts. We demonstrate that both dinoflagellate and animal cells have the capacity to rapidly fix nitrogen from seawater enriched in ammonium (in less than one hour). Further, by establishing the relative strengths of the capability to assimilate nitrogen for each cell compartment, we infer that dinoflagellate symbionts can fix 14 to 23 times more nitrogen than their coral host cells in response to a sudden pulse of ammoniumenriched seawater. Given the importance of nitrogen in cell maintenance, growth and functioning, the capability to fix ammonium from seawater into the symbiotic system may be a key component of coral nutrition. Interestingly, this metabolic response appears to be triggered rapidly by episodic nitrogen availability. The methods and results presented in this study open up for the exploration of dynamics and spatial patterns associated with metabolic activities and nutritional interactions in a multitude of organisms that live in symbiotic relationships.

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Primary site and initial products of ammonium assimilation in the symbiotic sea anemone Anemonia viridis

Cited by 46 publications

References 41 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

Diazotrophs: Overlooked Key Players within the Coral Symbiosis and Tropical Reef Ecosystems?

A single-cell view of ammonium assimilation in coral–dinoflagellate symbiosis

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