Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30–150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ15N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a, lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.

With coral reefs declining globally, resilience of these ecosystems hinges on successful coral recruitment. However, knowledge of the acclimatory and/or adaptive potential in response to environmental challenges such as ocean acidification (OA) in earliest life stages is limited. Our combination of physiological measurements, microscopy, computed tomography techniques and gene expression analysis allowed us to thoroughly elucidate the mechanisms underlying the response of early-life stages of corals, together with their algal partners, to the projected decline in oceanic pH. We observed extensive physiological, morphological and transcriptional changes in surviving recruits, and the transition to a less-skeleton/more-tissue phenotype. We found that decreased pH conditions stimulate photosynthesis and endosymbiont growth, and gene expression potentially linked to photosynthates translocation. Our unique holistic study discloses the previously unseen intricate net of interacting mechanisms that regulate the performance of these organisms in response to OA.

Depth related parameters, specifically light, affect different aspects of corals physiology, including fluorescence. Green fluorescence protein (GFP)-like pigments found in many coral species have been suggested to serve a variety of functions, including photo-protection and photo-enhancement. Using fluorescence imaging and molecular analysis, we further investigated the role of these proteins on the physiology of the coral Stylophora pistillata and its algal partners. Fluorescence was found to differ significantly between depths for larvae and adult colonies. Larvae from the shallow reef presented a higher GFP expression and a greater fluorescence intensity compared to the larvae from the mesophotic reef, reflecting the elevated need for photo-protection against high light levels characteristic of the shallow reef, thus supporting the "sunscreen" hypothesis. Additionally, given the lower but still occurring protein expression under non-damaging low light conditions, our results suggest that GFP-like proteins might act to regulate the amount of photosynthetically usable light for the benefit of the symbiotic algae. Moreover, we propose that the differences in GFP expression and green fluorescence between shallow and deep larvae indicate that the GFPs within coral larvae might serve to attract and retain different symbiont clades, increasing the chances of survival when encountering new environments.

In light of the chronic stress and mass mortality reef-building corals face under climate change, it is critical to understand the processes essential to reef persistence and replenishment, including coral reproduction and development. Here we quantify gene expression and size sensitivity to ocean acidification across a set of developmental stages in the rice coral, Montipora capitata. Gametes and then embryos and swimming larvae were exposed to three pH treatments ranging from 7.8 (Ambient), 7.6 (Low) and 7.3 (Xlow) from fertilization to 9 days post-fertilization. Embryo development and size, planula volume, and stage-specific gene expression were compared between treatments at each stage to determine the effects of acidified seawater on early development. While there was no measurable size differentiation between fertilized eggs and embryos at the prawn chip stage exposed to ambient, low, and extreme low pH, early gastrula and planula raised in reduced pH treatments were significantly smaller than those raised in ambient seawater, suggesting an energetic cost to developing under low pH. However, no differentially expressed genes emerged between treatments at any time point, except swimming larvae. Larvae from pH 7.6 showed upregulation of genes involved in cell division, regulation of transcription, lipid metabolism, and oxidative stress in comparison to the other two treatments, and smallest sizes in this treatment. While low pH appears to increase energetic demands and trigger oxidative stress, the developmental process is robust to this at a molecular level, with swimming larval stage reached in all pH treatments.

The integrity of coral reefs worldwide is jeopardized by ocean acidification (OA). Most studies conducted so far have focused on the vulnerability to OA of corals inhabiting shallow reefs while nothing is currently known about the response of mesophotic scleractinian corals. In this study, we assessed the susceptibility to OA of corals, together with their algal partners, inhabiting a wide depth range. We exposed fragments of the depth generalist coral Stylophora pistillata collected from either 5 or 45 m to simulated future OA conditions, and assessed key molecular, physiological and photosynthetic processes influenced by the lowered pH. Our comparative analysis reveals that mesophotic and shallow S. pistillata corals are genetically distinct and possess different symbiont types. Under the exposure to acidification conditions, we observed a 50% drop of metabolic rate in shallow corals, whereas mesophotic corals were able to maintain unaltered metabolic rates. Overall, our gene expression and physiological analyses show that mesophotic corals possess a greater capacity to cope with the effects of OA compared to their shallow counterparts. Such capability stems from physiological characteristics (i.e., biomass and lipids energetics), a greater capacity to regulate cellular acid-base parameters, and a higher baseline expression of cell adhesion and extracellular matrix genes. Moreover, our gene expression analysis suggests that the enhanced symbiont photochemical efficiency under high pCO 2 levels could prevent acidosis of the host cells and it could support a greater translocation of photosynthates, increasing the energy pool available to the host. With this work, we provide new insights on the response to OA of corals living at mesophotic depths. Our investigation discloses key genetic and physiological traits underlying the potential for corals to cope with future OA conditions.

As the devastating impacts of global climate change and local anthropogenic stressors on shallow-water coral reefs are expected to rise, mesophotic coral ecosystems have increasingly been regarded as potential lifeboats for coral survival, providing a source of propagules to replenish shallower reefs. Yet, there is still limited knowledge of the capacity for coral larvae to adjust to light intensities that change with depth. This study elucidates the mechanisms underlying plasticity during early life stages of the coral Porites astreoides that enable survival across broad depth gradients. We examined physiological and morphological variations in larvae from shallow (8–10 m) and mesophotic (45 m) reefs in Bermuda, and evaluated differences in survival, settlement patterns and size among recruits depending on light conditions using a reciprocal ex situ transplantation experiment. Larvae released from mesophotic adults were found to have significantly lower respiration rates and were significantly larger than those derived from shallow adults, indicating higher content of energetic resources and suggesting a greater dispersal potential for mesophotic larvae compared to their shallow counterparts. Additionally, larvae released from mesophotic adults experienced higher settlement success and larger initial spat size compared to larvae from shallow adults, demonstrating a potential connection between parental origin, offspring quality, and recruitment success. Although both shallow and mesophotic larvae exhibited the capacity to survive and settle under reciprocal light conditions, all larvae had higher survival under mesophotic light conditions regardless of parental origin, suggesting that conditions experienced under low light may enable longer larval life, further extending the dispersal period. These results indicate that larvae from mesophotic Porites astreoides colonies are likely capable of reseeding shallow reefs in Bermuda, thereby supporting the Deep Reef Refugia Hypothesis.

Understanding the formation of the coral skeleton has been a common subject uniting various marine and materials study fields. Two main regions dominate coral skeleton growth: Rapid Accretion Deposits (RADs) and Thickening Deposits (TDs). These have been extensively characterized at the 2D level, but their 3D characteristics are still poorly described. Here, we present an innovative approach to combine synchrotron phase contrast-enhanced microCT (PCE-CT) with artificial intelligence (AI) to explore the 3D architecture of RADs and TDs within the coral skeleton. As a reference study system, we used recruits of the stony coral Stylophora pistillata from the Red Sea, grown under both natural and simulated ocean acidification conditions. We thus studied the recruit’s skeleton under both regular and morphologically-altered acidic conditions. By imaging the corals with PCE-CT, we revealed the interwoven morphologies of RADs and TDs. Deep-learning neural networks were invoked to explore AI segmentation of these regions, to overcome limitations of common segmentation techniques. This analysis yielded highly-detailed 3D information about the RAD’s and TD’s architecture. Our results demonstrate how AI can be used as a powerful tool to obtain 3D data essential for studying coral biomineralization and for exploring the effects of environmental change on coral growth.

The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness.