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Abstract Corals access inorganic seawater nutrients through their autotrophic endosymbiotic dinoflagellates, but also capture planktonic prey through heterotrophic feeding. Introduction The immense biodiversity and productivity of tropical coral reefs exists in a marine environment that is generally characterized by low nutrient levels and plankton concentrations. Results and Discussion The ultrastructural fate of autotrophic C and N Consistent with previous studies in other corals 38 , 40 , fixed and assimilated DIC was primarily deposited in primary and secondary starch deposits and lipid bodies in the symbiont, and as translocated product in the host lipid bodies of the coral gastrodermis Fig.
Open in a separate window. Figure 1. Figure 2. Figure 3. Figure 4. Figure 5. Figure 6. Autotrophic vs. Figure 7. Elevated temperature reduces nutrient input and alters partitioning between tissue compartments Elevated temperature consistently reduced nutrient assimilation in all compartments for both modes of nutrition Fig. Table 1 The effect of temperature on autotrophic and heterotrophic input. Aut [F] vs.
Conclusions By employing correlative TEM-NanoSIMS isotopic imaging, our study revealed the primary sites for the concentration and storage of nutrients derived from the two main fundamental modes of coral nutrition, auto- and heterotrophy.
Figure 8. Isotopic labelling of Artemia sp. Statistical analysis Considering that ROI enrichment values contain two sources of variability, resulting from the cutting level within the cell affecting for example the abundance of starch granules in a particular symbiont ROI and the true biological variability as result of size, age and physiological state of individual cells, we decided to treat the ROI data points as raw data points and include biological replicate as a factor in the analysis, rather than treating multiple ROIs from one biological replicate as technical replicates and reducing them to a single value.
Electronic supplementary material Supplementary Figures and Tables 1. Author Contributions T. Notes Competing Interests The authors declare no competing interests. Footnotes Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations. Contributor Information Thomas Krueger, Email: hc. Electronic supplementary material Supplementary information accompanies this paper at References 1.
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A re-allocation of energy to repair injured zones has often been observed in plant-myccorhizal associations 48 , 49 or even in coral-endolith 50 and coral-dinoflagellate 36 , 38 associations. Nevertheless, despite retaining carbon for their own growth, symbionts of unfed S.
Contrary to unfed corals, normal nutritional exchanges between symbionts and the host in fed corals resumed as soon as the heat stress stopped. This restoration of photosynthate translocation ca. The importance of external food supply for the maintenance of symbiont concentration and photosynthetic activity has been observed several times This observation suggests that heterotrophic nutrients cannot entirely sustain symbiont needs during heat stress either because S.
In a previous study, Tremblay et al. Collectively, these results suggest that carbon exchange is asymmetric between coral host and symbionts, and that bleaching can arise when nutrient allocation to symbionts is insufficient to afford the costs of repair mechanisms. In general, across many ecosystems and organisms, there is a tight coupling between rates of photosynthesis and respiration 52 , 53 , 54 , such that animal respiration decreases in response to declining photosynthetic carbon supply 52 , but it is not always the case Such an increase in energy expenditure on tissue maintenance during heat stress, so that enough adenosine triphosphate ATP is produced to sustain routine metabolism, has previously been observed It appears that these metabolic adjustments maintained the metabolic balance i.
The additional energy needed to cover these costs was partially obtained by heterotrophy in fed colonies, whereas energy supply and reserves were restricted in unfed colonies, and these colonies, therefore, experienced significant bleaching during the recovery period. The carbon budgets of S. The higher rates of respiration in fed colonies may have contributed to a higher supply of metabolic CO 2 to the symbionts, thereby maintaining a higher symbiotic stability 58 , Metabolic re-adjustments came at the expense of calcification for both fed and unfed colonies during heat stress, highlighting that biomineralization is an energetically costly process Calcification was not directly related to respiration rates, but rather was associated with photosynthetic and carbon translocation rates.
In addition, calcification rate was related to heterotrophic feeding 61 , with rates 1. Heterotrophy could affect calcification directly through the supply of organic molecules or energy necessary to the building of the organic matrix 62 , or it might affect calcification indirectly by enhancing photosynthesis. These results suggest that heterotrophic feeding does not alter the sensitivity of corals to heat stress, as previously observed in corals under acidification stress 63 , 64 , 65 , Our observation is also in contrast to other studies demonstrating that supply of inorganic nutrients can reduce calcification sensitivity to both heat stress and to ocean acidification 66 , 67 , 68 , The most likely explanation for these contrasting results is that inorganic nutrients are primarily taken up by symbionts, whereas organic nutrients feeding are acquired by the host and a small fraction is subsequently shared with the symbionts.
As calcification is related to photosynthesis, and photosynthesis is enhanced by inorganic nutrient supply, provision of inorganic nutrients can prevent decreases in calcification during heat stress. We hypothesize that the difference in calcification observed is linked to the quality of the photosynthates produced. Stress-induced changes in exopolysaccharide composition and production have been observed in cyanobacteria 70 , and the same could potentially occur in corals.
A better knowledge of the effect of photosynthate quality on calcification rates will provide new insight into the effect of climate change on coral calcification. This work has applied multiple tools physiological and isotopic labeling approaches to the study of host-symbiont interactions and has revealed new data to illustrate how heat stress and heterotrophy interact, with implications for reef coral ecology in the midst of global change.
By combining pulse-chase stable-isotopic labeling 13 C with physiological measurements, we have thus quantified the acquisition and allocation of carbon and nutrients within a coral-dinoflagellate symbiosis during a heat stress event.
These results demonstrate that an elevation in seawater temperature induces a shift in carbon allocation toward retention of carbon by the symbionts and, consequently, decreased the amount of carbon translocated to the coral host. Provision of particulate matter as a heterotrophic food source for the coral host contributed to restoring the normal nutritional relationships between host and symbionts, but it did not mitigate the effects of temperature stress on coral calcification and growth rates.
More broadly these results suggest that coral calcification, and the net accretion of coral reefs, is likely to be severely impacted as heat stress events intensifies in the future.
A total of nubbins were prepared by cutting the apical branches of four large colonies 52 nubbins per colony of the scleractinian coral Stylophora pistillata originating from the Red Sea. During this period, all nubbins were fed twice a week with Artemia salina nauplii 2, nauplii per tank per feeding event The total daily light integral received by our corals in these conditions A typical sunny day generates a total of Water temperature was adjusted to Before the start of the experiment, feeding was ceased in four of the eight tanks, and these nubbins were maintained unfed for five weeks.
Nubbins in the remaining four tanks were fed three times a week with A. After the preparation of fed and unfed nubbins, a set of initial measurements, described below, was performed in all tanks called day 0, see Supplementary Information.
Then, four different treatments with two tanks per treatment were established using a factorial design: nubbins were either kept unfed or fed at a control temperature of Temperature was increased over 10 days, which corresponds to the temperature variations occurring in some reef flats or during low tide conditions 73 , 74 , In the HTF and HTU tanks, heat stress was maintained for four weeks until a decrease in the photosynthetic efficiency of the corals under heat stress was monitored , after which a set of measurements were performed in all tanks called day Temperature was then decreased over one week back to A set of final measurements was performed in all tanks at the end of the fourth week of recovery called day Calcification rates were determined at each sampling time day 0, day 28 and day 56 for the same four nubbins per treatment two nubbins per tank from four colonies , using the buoyant weight technique Rates of respiration R and net photosynthesis P n were measured using four nubbins per treatment two nubbins per tank from four colonies at each sampling time.
Seawater temperature in the chambers was maintained at Rates of gross photosynthesis P g were calculated by adding R to P n. Samples were then frozen for later determinations of symbiont concentration using an inverted microscope Leica, Wetzlar, Germany and the Histolab 5. To apportion holobiont respiration into symbiont and host components, the respiration rates of freshly isolated symbionts R S were determined for four nubbins per treatment two nubbins per tank from four colonies at each sampling time.
The supernatant was discarded, and the symbionts were re-suspended in FSW. Respiration rates and symbiont concentration were measured as described above. H 13 CO 3 labeling experiments were performed according to Tremblay et al.
The medium was continuously stirred and maintained at All nubbins were treated according to Tremblay et al. Briefly, tissue was detached from the skeleton using an air-brush in FSW. The slurry was homogenised using a potter tissue grinder and centrifuged to separate coral host and symbionts. Samples were flash-frozen in liquid nitrogen and freeze-dried until analysis.
The equations used to calculate the autotrophic carbon budget are fully described in Tremblay et al. See Table 5 for a list of symbols and their definitions. All data were normalized to the skeletal surface area using the wax technique The percentages of autotrophic carbon contributing to the total respiration of the holobiont CZAR have been assessed in each treatment 19 , The percentages of autotrophic and heterotrophic carbon contributing to the respiration of the host CTAR and CHAR respectively have also been assessed.
Data were transformed with a natural logarithm transformation when required i. The tank effect nested within temperature and feeding was not significant for any of the parameters, it was therefore excluded from analyses. The two tanks per temperature and feeding were pooled, according to the procedure described in Underwood 80 , to check that variation among experimental units was zero, and that pooling was appropriate and did not change the conclusion of the analysis.
Linear regressions, using standard least-squares techniques, were used to estimate the relationship between the mean of P C or T S and the mean of C C or R C. How to cite this article : Tremblay, P. Heterotrophy promotes the re-establishment of photosynthate translocation in a symbiotic coral after heat stress. Publisher's note: Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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