Nutrient starvation and nitrate pollution impairs the assimilation of dissolved organic phosphorus in coral-Symbiodiniaceae symbiosis.

Phosphorus (P) is an essential but limiting nutrient for coral growth due to low concentrations of dissolved inorganic concentrations (DIP) in reef waters. P limitation is often exacerbated when concentrations of dissolved inorganic nitrogen (DIN) increase in the reef. To increase their access to phosphorus, corals can use organic P dissolved in seawater (DOP). They possess phosphatase enzymes that transform DOP into DIP, which can then be taken up by coral symbionts. Although the concentration of DOP in reef waters is much higher than DIP, the dependence of corals on this P source is still poorly understood, especially with different concentrations of DIN in seawater. As efforts to predict the future of corals increase, improved knowledge of the P requirements of corals living under different DIN concentrations may be key to predicting coral health. In this study, we investigated P content and phosphatase activities (PAs) in Stylophora pistillata maintained under nutrient starvation, long-term nitrogen enrichment (nitrate or ammonium at 2 µM) and short-term (few hours) nitrogen pulses. Results show that under nutrient depletion and ammonium-enriched conditions, a significant increase in PAs was observed compared to control conditions, with no change in the N:P ratio of the coral tissue. On the contrary, under nitrate enrichment, there was no increase in PAs compared to control conditions, but an increase in the N:P ratio of the coral tissue. These results suggest that under nitrate enrichment, corals were unable to increase their ability to rely on DOP and replenish their cellular P content. An increase in cellular N:P ratio is detrimental to coral health as it increases the susceptibility of coral bleaching under thermal stress. These results provide an overall view of the P requirements of corals exposed to different nutrient conditions and improve our understanding of the effects of nitrogen enrichment on corals.

Limited phosphorus availability is the Achilles heel of tropical reef corals in a warming ocean.

During the 20(th) 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.

On the use of 31P NMR for the quantification of hydrosoluble phosphorus-containing compounds in coral host tissues and cultured zooxanthellae.

(31)P Nuclear Magnetic Resonance (NMR) was assessed to investigate the phosphorus-containing compounds present in the tissues of the scleractinian coral Stylophora pistillata as well as of cultured zooxanthellae (CZ). Results showed that phosphorus-containing compounds observed in CZ were mainly phosphate and phosphate esters. Phosphate accounted for 19 ± 2% of the total phosphorus compounds observed in CZ maintained under low P-levels (0.02 µM). Adding 5 mM of dissolved inorganic phosphorus (KH2PO4) to the CZ culture medium led to a 3.1-fold increase in intracellular phosphate, while adding 5 mM of dissolved organic phosphorus led to a reduction in the concentration of phosphorus compounds, including a 2.5-fold intracellular phosphate decrease. In sharp contrast to zooxanthellae, the host mainly contained phosphonates, and to a lesser extent, phosphate esters and phosphate. Two-months of host starvation decreased the phosphate content by 2.4 fold, while bleaching of fed corals did not modify this content. Based on (31)P NMR analyses, this study highlights the importance of phosphonates in the composition of coral host tissues, and illustrates the impact of phosphorus availability on the phosphorus composition of host tissues and CZ, both through feeding of the host and inorganic phosphorus enrichment of the CZ.

New insights into carbon acquisition and exchanges within the coral-dinoflagellate symbiosis under NH4+ and NO3- supply.

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 µM), a 3 µM nitrate enrichment induced a significant decrease in carbon fixation rate and low values of carbon translocation, compared with control conditions (N : P = 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 = 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.

Coral uptake of inorganic phosphorus and nitrogen negatively affected by simultaneous changes in temperature and pH.

The effects of ocean acidification and elevated seawater temperature on coral calcification and photosynthesis have been extensively investigated over the last two decades, whereas they are still unknown on nutrient uptake, despite their importance for coral energetics. We therefore studied the separate and combined impacts of increases in temperature and pCO(2) on phosphate, ammonium, and nitrate uptake rates by the scleractinian coral S. pistillata. Three experiments were performed, during 10 days i) at three pH(T) conditions (8.1, 7.8, and 7.5) and normal temperature (26°C), ii) at three temperature conditions (26°, 29°C, and 33°C) and normal pH(T) (8.1), and iii) at three pH(T) conditions (8.1, 7.8, and 7.5) and elevated temperature (33°C). After 10 days of incubation, corals had not bleached, as protein, chlorophyll, and zooxanthellae contents were the same in all treatments. However, photosynthetic rates significantly decreased at 33°C, and were further reduced for the pH(T) 7.5. The photosynthetic efficiency of PSII was only decreased by elevated temperature. Nutrient uptake rates were not affected by a change in pH alone. Conversely, elevated temperature (33°C) alone induced an increase in phosphate uptake but a severe decrease in nitrate and ammonium uptake rates, even leading to a release of nitrogen into seawater. Combination of high temperature (33°C) and low pH(T) (7.5) resulted in a significant decrease in phosphate and nitrate uptake rates compared to control corals (26°C, pH(T) = 8.1). These results indicate that both inorganic nitrogen and phosphorus metabolism may be negatively affected by the cumulative effects of ocean warming and acidification.