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Climate change accelerates coral reef decline and jeopardizes recruitment essential for ecosystem recovery. Adult corals rely on a vital nutritional exchange with their symbiotic algae (Symbiodiniaceae), but the dynamics of reliance from fertilization to recruitment are understudied. We investigated the physiological, metabolomic, and transcriptomic changes across 13 developmental stages of Montipora capitata, a coral in Hawaiʻi that inherits symbionts from parent to egg. We found that embryonic development depends on maternally provisioned mRNAs and lipids, with a rapid shift to symbiont-derived nutrition in late developmental stages. Symbiont density and photosynthesis peak in swimming larvae to fuel pelagic dispersal. By contrast, respiratory demand increases significantly during metamorphosis and settlement, reflecting this energy-intensive morphological reorganization. Symbiont proliferation is driven by symbiont ammonium assimilation in larval stages with little evidence of nitrogen metabolism in the coral host. As development progresses, the host enhances nitrogen sequestration, regulating symbiont populations, and ensuring the transfer of fixed carbon to support metamorphosis, with both metabolomic and transcriptomic indicators of increased carbohydrate availability. Although algal symbiont community composition remained stable, bacterial communities shifted with ontogeny, associated with holobiont metabolic reorganization. Our study reveals extensive metabolic changes during development with increasing reliance on symbiont nutrition. Metamorphosis and settlement emerge as critical periods of energetic vulnerability to projected climate scenarios that destabilize symbiosis. This highly detailed characterization of symbiotic nutritional exchange during sensitive early life stages provides essential knowledge for understanding and forecasting the function of nutritional symbioses and, specifically, coral survival and recruitment in a future of climate change. 

Rising sea surface temperatures are increasingly causing breakdown in the nutritional relationship between corals and algal endosymbionts (Symbiodiniaceae), threatening the basis of coral reef ecosystems and highlighting the critical role of coral reproduction in reef maintenance. The effects of thermal stress on metabolic exchange (i.e., transfer of fixed carbon photosynthates from symbiont to host) during sensitive early life stages, however, remains understudied. We exposed symbiotic Montipora capitata coral larvae in Hawaiʻi to high temperature (+2.5°C for 3 days), assessed rates of photosynthesis and respiration, and used stable isotope tracing (4 mM 13C sodium bicarbonate; 4.5 h) to quantify metabolite exchange. While larvae did not show any signs of bleaching and did not experience declines in survival and settlement, metabolic depression was significant under high temperature, indicated by a 19% reduction in respiration rates, but with no change in photosynthesis. Larvae exposed to high temperature showed evidence for maintained translocation of a major photosynthate, glucose, from the symbiont, but there was reduced metabolism of glucose through central carbon metabolism (i.e., glycolysis). The larval host invested in nitrogen cycling by increasing ammonium assimilation, urea metabolism, and sequestration of nitrogen into dipeptides, a mechanism that may support the maintenance of glucose translocation under thermal stress. Host nitrogen assimilation via dipeptide synthesis appears to be used for nitrogen limitation to the Symbiodiniaceae, and we hypothesize that nitrogen limitation contributes to retention of fixed carbon by favoring photosynthate translocation to the host. Collectively, our findings indicate that although these larvae are susceptible to metabolic stress under high temperature, diverting energy to nitrogen assimilation to maintain symbiont population density, photosynthesis, and carbon translocation may allow larvae to avoid bleaching and highlights potential life stage specific metabolic responses to stress. 

Corals form symbiotic relationships with dinoflagellate algae of the family Symbiodiniaceae, bacteria, and other microbes. Central to that relationship is the regulation of nutrition flux between the animal host and the photosynthetic Symbiodiniaceae that it is reliant on for the majority of metabolic needs. Nitrogen availability controls the growth and density of Symbiodiniaceae within coral tissues and has been proposed to play a role in host derived symbiosis regulation. Warming ocean temperatures and subsequent increases in dissolved organic carbon can potentially increase nitrogen fixation and lead to bleaching. We investigated the importance of nitrogen metabolism in vivo with LC-MS based stable isotope tracing using nubbins from three species of Hawaiian coral, the more heat tolerant Montipora capitata and Porites compressa and the more heat sensitive Pocillopora acuta , that were collected from reefs in Kāne’ohe Bay, O’ahu. In addition to 15 N incorporation into nucleotides, amino acids, and urea cycle metabolites, we also observed significant isotopic labeling in dipeptides, supporting their previous identification as major heat stress response metabolites. Surprisingly, the dipeptides are highly enriched in 15 N compared to free amino acids, which are the biosynthetic precursors for dipeptides. This suggests that there is a high turnover of dipeptide pools and distinct biosynthetic mechanisms that separately mediate amino acid and dipeptide production. These preliminary data show that nitrogen assimilation in the coral holobiont is likely compartmentalized, with rapid assimilation and quick dipeptide turnover occurring in one region of the holobiont and slow turnover of other nitrogen containing metabolites in other region(s). 

Urgent action is needed to prevent the demise of coral reefs as the climate crisis leads to an increasingly warmer and more acidic ocean. Propagating climate change–resistant corals to restore degraded reefs is one promising strategy; however, empirical evidence is needed to determine whether stress resistance is affected by transplantation beyond a coral’s native reef. Here, we assessed the performance of bleaching-resistant individuals of two coral species following reciprocal transplantation between reefs with distinct pH, salinity, dissolved oxygen, sedimentation, and flow dynamics to determine whether heat stress response is altered following coral exposure to novel physicochemical conditions in situ. Critically, transplantation had no influence on coral heat stress responses, indicating that this trait was relatively fixed. In contrast, growth was highly plastic, and native performance was not predictive of performance in the novel environment. Coral metabolic rates and overall fitness were higher at the reef with higher flow, salinity, sedimentation, and diel fluctuations of pH and dissolved oxygen, and did not differ between native and cross-transplanted corals, indicating acclimatization via plasticity within just 3 mo. Conversely, cross-transplants at the second reef had higher fitness than native corals, thus increasing the fitness potential of the recipient population. This experiment was conducted during a nonbleaching year, so the potential benefits to recipient population fitness are likely enhanced during bleaching years. In summary, this study demonstrates that outplanting bleaching-resistant corals is a promising tool for elevating the resistance of coral populations to ocean warming. 

Abstract Ocean warming is causing global coral bleaching events to increase in frequency, resulting in widespread coral mortality and disrupting the function of coral reef ecosystems. However, even during mass bleaching events, many corals resist bleaching despite exposure to abnormally high temperatures. While the physiological effects of bleaching have been well documented, the consequences of heat stress for bleaching‐resistant individuals are not well understood. In addition, much remains to be learned about how heat stress affects cellular‐level processes that may be overlooked at the organismal level, yet are crucial for coral performance in the short term and ecological success over the long term. Here we compared the physiological and cellular responses of bleaching‐resistant and bleaching‐susceptible corals throughout the 2019 marine heatwave in Hawai'i, a repeat bleaching event that occurred 4 years after the previous regional event. Relative bleaching susceptibility within species was consistent between the two bleaching events, yet corals of both resistant and susceptible phenotypes exhibited pronounced metabolic depression during the heatwave. At the cellular level, bleaching‐susceptible corals had lower intracellular pH than bleaching‐resistant corals at the peak of bleaching for both symbiont‐hosting and symbiont‐free cells, indicating greater disruption of acid–base homeostasis in bleaching‐susceptible individuals. Notably, cells from both phenotypes were unable to compensate for experimentally induced cellular acidosis, indicating that acid–base regulation was significantly impaired at the cellular level even in bleaching‐resistant corals and in cells containing symbionts. Thermal disturbances may thus have substantial ecological consequences, as even small reallocations in energy budgets to maintain homeostasis during stress can negatively affect fitness. These results suggest concern is warranted for corals coping with ocean acidification alongside ocean warming, as the feedback between temperature stress and acid–base regulation may further exacerbate the physiological effects of climate change.