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.
SUMMARYCorals live in symbiosis with dinoflagellates of the genus Symbiodinum. These dinoflagellates translocate a large part of the photosynthetically fixed carbon to the host, which in turn uses it for its own needs. Assessing the carbon budget in coral tissue is a central question in reef studies that still vexes ecophysiologists. The amount of carbon fixed by the symbiotic association can be determined by measuring the rate of photosynthesis, but the amount of carbon translocated by the symbionts to the host and the fate of this carbon are more difficult to assess. In the present study, we propose a novel approach to calculate the budget of autotrophic carbon in the tissue of scleractinian corals, based on a new model and measurements made with the stable isotope 13 C. Colonies of the scleractinian coral Stylophora pistillata were incubated in H 13 CO 3 --enriched seawater, after which the fate of 13 C was followed in the symbionts, the coral tissue and the released particulate organic carbon (i.e. mucus). Results obtained showed that after 15min, ca. 60% of the carbon fixed was already translocated to the host, and after 48h, this value reached 78%. However, ca. 48% of the photosynthetically fixed carbon was respired by the symbiotic association, and 28% was released as dissolved organic carbon. This is different from other coral species, where <1% of the total organic carbon released is from newly fixed carbon. Only 23% of the initially fixed carbon was retained in the symbionts and coral tissue after 48h. Results show that our 13 C-based model could successfully trace the carbon flow from the symbionts to the host, and the photosynthetically acquired carbon lost from the symbiotic association.
SUMMARYThis study was designed to assess the importance of dissolved free amino acids (DFAA) as a nitrogen source for the scleractinian coral Stylophora pistillata. For this purpose, experiments were performed using 15 N-enriched DFAAs, and % 15 N enrichment was measured both in animal tissue and zooxanthellae at different DFAA concentrations, incubation time and light levels. As previously observed for urea, which is another source of organic nitrogen, DFAA uptake exhibited a biphasic mode consisting of an active carrier-mediated transport for concentrations below 3·mol·l -1 and a linear uptake for higher concentrations. The value of the carrier affinity (K m =1.23·mol·l -1 DFAA) indicated good adaptation of the corals to the low levels of DFAA concentrations measured in most oligotrophic waters. DFAA uptake was also correlated with light. The DFAA contribution to the nitrogen requirements for tissue growth was compared to the contribution of ammonia, nitrate and urea, for which uptake was also measured in S. pistillata. Inorganic sources (NH 4 + and NO 3 -) contributed 75% of the daily nitrogen needs against 24% for organic sources. Taken altogether, dissolved organic and inorganic nitrogen can supply almost 100% of the nitrogen needs for tissue growth.
Anthropogenic nutrient enrichment affects the biogeochemical cycles and nutrient stoichiometry of coastal ecosystems and is often associated with coral reef decline. However, the mechanisms by which dissolved inorganic nutrients, and especially nitrogen forms (ammonium versus nitrate) can disturb the association between corals and their symbiotic algae are subject to controversial debate. Here, we investigated the coral response to varying N : P ratios, with nitrate or ammonium as a nitrogen source. We showed significant differences in the carbon acquisition by the symbionts and its allocation within the symbiosis according to nutrient abundance, type and stoichiometry. In particular, under low phosphate concentration (0.05 mM), a 3 mM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P ¼ 0.5 : 0.05), while these processes were significantly enhanced when nitrate was replaced by ammonium. A combined enrichment in ammonium and phosphorus (N : P ¼ 3 : 1) induced a shift in nutrient allocation to the symbionts, at the detriment of the host. Altogether, these results shed light into the effect of nutrient enrichment on reef corals. More broadly, they improve our understanding of the consequences of nutrient loading on reef ecosystems, which is urgently required to refine risk management strategies.
Symbiotic scleractinian corals are particularly affected by climate change stress and respond by bleaching (losing their symbiotic dinoflagellate partners). Recently, the energetic status of corals is emerging as a particularly important factor that determines the corals’ vulnerability to heat stress. However, detailed studies of coral energetic that trace the flow of carbon from symbionts to host are still sparse. The present study thus investigates the impact of heat stress on the nutritional interactions between dinoflagellates and coral Stylophora pistillata maintained under auto- and heterotrophy. First, we demonstrated that the percentage of autotrophic carbon retained in the symbionts was significantly higher during heat stress than under non-stressful conditions, in both fed and unfed colonies. This higher photosynthate retention in symbionts translated into lower rates of carbon translocation, which required the coral host to use tissue energy reserves to sustain its respiratory needs. As calcification rates were positively correlated to carbon translocation, a significant decrease in skeletal growth was observed during heat stress. This study also provides evidence that heterotrophic nutrient supply enhances the re-establishment of normal nutritional exchanges between the two symbiotic partners in the coral S. pistillata, but it did not mitigate the effects of temperature stress on coral calcification.
During the 20th century, seawater temperatures have significantly increased, leading to profound alterations in biogeochemical cycles and ecosystem processes. Elevated temperatures have also caused massive bleaching (symbiont/pigment loss) of autotrophic symbioses, such as in coral-dinoflagellate association. As symbionts provide most nutrients to the host, their expulsion during bleaching induces host starvation. However, with the exception of carbon, the nutritional impact of bleaching on corals is still unknown, due to the poorly understood requirements in inorganic nutrients during stress. We therefore assessed the uptake rates of nitrogen and phosphate by five coral species maintained under normal and thermal stress conditions. Our results showed that nitrogen acquisition rates were significantly reduced during thermal stress, while phosphorus uptake rates were significantly increased in most species, suggesting a key role of this nutrient. Additional experiments showed that during thermal stress, phosphorus was required to maintain symbiont density and photosynthetic rates, as well as to enhance the translocation and retention of carbon within the host tissue. These findings shed new light on the interactions existing between corals and inorganic nutrients during thermal stress, and highlight the importance of phosphorus for symbiont health.
Nitrogen (N) is a limiting nutrient in vast regions of the world's oceans, yet the sources of N available to various phytoplankton groups remain poorly understood. In this study, we investigated inorganic carbon (C) fixation rates and nitrate (NO 3 −), ammonium (NH 4 +) and urea uptake rates at the single cell level in photosynthetic pico-eukaryotes (PPE) and the cyanobacteria Prochlorococcus and Synechococcus. To that end, we used dual 15 N and 13 C-labeled incubation assays coupled to flow cytometry cell sorting and nanoSIMS analysis on samples collected in the North Pacific Subtropical Gyre (NPSG) and in the California Current System (CCS). Based on these analyses, we found that photosynthetic growth rates (based on C fixation) of PPE were higher in the CCS than in the NSPG, while the opposite was observed for Prochlorococcus. Reduced forms of N (NH 4 + and urea) accounted for the majority of N acquisition for all the groups studied. NO 3 − represented a reduced fraction of total N uptake in all groups but was higher in PPE (17.4 ± 11.2% on average) than in Prochlorococcus and Synechococcus (4.5 ± 6.5 and 2.9 ± 2.1% on average, respectively). This may in part explain the contrasting biogeography of these picoplankton groups. Moreover, single cell analyses reveal that cell-to-cell heterogeneity within picoplankton groups was significantly greater for NO 3 − uptake than for C fixation and NH 4 + uptake. We hypothesize that cellular heterogeneity in NO 3 − uptake within groups facilitates adaptation to the fluctuating availability of NO 3 − in the environment.
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