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The relationship between corals and dinoflagellates of the genus Symbiodinium is fundamental to the functioning of coral ecosystems. It has been suggested that reef corals may adapt to climate change by changing their dominant symbiont type to a more thermally tolerant one, although the capacity for such a shift is potentially hindered by the compatibility of different host-symbiont pairings. Here we combined transcriptomic and metabolomic analyses to characterize the molecular, cellular, and physiological processes that underlie this compatibility, with a particular focus on Symbiodinium trenchii, an opportunistic, thermally tolerant symbiont that flourishes in coral tissues after bleaching events. Symbiont-free individuals of the sea anemone Exaiptasia pallida (commonly referred to as Aiptasia), an established model system for the study of the cnidarian-dinoflagellate symbiosis, were colonized with the “normal” (homologous) symbiont Symbiodinium minutum and the heterologous S. trenchii. Analysis of the host gene and metabolite expression profiles revealed that heterologous symbionts induced an expression pattern intermediate between the typical symbiotic state and the aposymbiotic state. Furthermore, integrated pathway analysis revealed that increased catabolism of fixed carbon stores, metabolic signaling, and immune processes occurred in response to the heterologous symbiont type. Our data suggest that both nutritional provisioning and the immune response induced by the foreign “invader” are important factors in determining the capacity of corals to adapt to climate change through the establishment of novel symbioses.

Oxidative stress inside cells occurs when the production of reactive oxygen species (ROS) is no longer efficiently counterbalanced by the generation of antioxidants. In this study, we measured the intracellular production of ROS, including hydrogen peroxide (H₂O₂), superoxide ( O 2 − ), and singlet oxygen (¹O₂), in cultured dinoflagellates of the genus Symbiodinium under thermal and oxidative stress. ROS tagged with fluorescent probes were measured by flow cytometry. Dissimilar Symbiodinium internal transcribed spacer 2 (ITS2) clades or phylotypes (A1, B2, E, F1) produced ROS in different quantities in response to stress. For example, when comparing the control (26 °C) to the high-temperature treatment (35 °C), Symbiodinium E showed no change in the intracellular concentrationsofanyoftheROS; butphylotypeA1displayeda10-fold increase in the overall ROS concentration and a 4-fold increase in O 2 − . Under oxidative stress, when 8 mmol l⁻¹ H₂O₂ was added to the cells, these same two Symbiodinium phylotypes increased their overall concentrations of ROS, but only Symbiodinium E showed an increase in the concentrations of O 2 − (2x) and ¹O₂ (3x). Therefore, not only were the stress responses of the various Symbiodinium phylotypes different but also the responses of individual phylotypes to thermal and oxidative stress were different in terms of ROS production. Variation in the quality and quantity of ROS generation and its implications for subsequent antioxidant production suggest that different stress mechanisms are at play. While our experiments were done under laboratory conditions that did not necessarily mirror ecological ones, these results provide new insight into processes inside Symbiodinium cells during stress events and add new explanations for a phylotype’s susceptibility to stress.

Diseases often display complex and distinct associations with their environment due to differences in etiology, modes of transmission between hosts, and the shifting balance between pathogen virulence and host resistance. Statistical modeling has been underutilized in coral disease research to explore the spatial patterns that result from this triad of interactions. We tested the hypotheses that: 1) coral diseases show distinct associations with multiple environmental factors, 2) incorporating interactions (synergistic collinearities) among environmental variables is important when predicting coral disease spatial patterns, and 3) modeling overall coral disease prevalence (the prevalence of multiple diseases as a single proportion value) will increase predictive error relative to modeling the same diseases independently. Four coral diseases: Porites growth anomalies (PorGA), Porites tissue loss (PorTL), Porites trematodiasis (PorTrem), and Montipora white syndrome (MWS), and their interactions with 17 predictor variables were modeled using boosted regression trees (BRT) within a reef system in Hawaii. Each disease showed distinct associations with the predictors. Environmental predictors showing the strongest overall associations with the coral diseases were both biotic and abiotic. PorGA was optimally predicted by a negative association with turbidity, PorTL and MWS by declines in butterflyfish and juvenile parrotfish abundance respectively, and PorTrem by a modal relationship with Porites host cover. Incorporating interactions among predictor variables contributed to the predictive power of our models, particularly for PorTrem. Combining diseases (using overall disease prevalence as the model response), led to an average six-fold increase in cross-validation predictive deviance over modeling the diseases individually. We therefore recommend coral diseases to be modeled separately, unless known to have etiologies that respond in a similar manner to particular environmental conditions. Predictive statistical modeling can help to increase our understanding of coral disease ecology worldwide.

Metabolite exchange is fundamental to the viability of the cnidarian–Symbiodiniaceae symbiosis and survival of coral reefs. Coral holobiont tolerance to environmental change might be achieved through changes in Symbiodiniaceae species composition, but differences in the metabolites supplied by different Symbiodiniaceae species could influence holobiont fitness. Using 13C stable-isotope labelling coupled to gas chromatography–mass spectrometry, we characterized newly fixed carbon fate in the model cnidarian Exaiptasia pallida (Aiptasia) when experimentally colonized with either native Breviolum minutum or non-native Durusdinium trenchii. Relative to anemones containing B. minutum, D. trenchii-colonized hosts exhibited a 4.5-fold reduction in 13C-labelled glucose and reduced abundance and diversity of 13C-labelled carbohydrates and lipogenesis precursors, indicating symbiont species-specific modifications to carbohydrate availability and lipid storage. Mapping carbon fate also revealed significant alterations to host molecular signalling pathways. In particular, D. trenchii-colonized hosts exhibited a 40-fold reduction in 13C-labelled scyllo-inositol, a potential interpartner signalling molecule in symbiosis specificity. 13C-labelling also highlighted differential antioxidant- and ammonium-producing pathway activities, suggesting physiological responses to different symbiont species. Such differences in symbiont metabolite contribution and host utilization may limit the proliferation of stress-driven symbioses; this contributes valuable information towards future scenarios that select in favour of less-competent symbionts in response to environmental change.

Rising seawater temperatures pose a significant threat to the persistence of coral reefs. Despite the importance of these systems, major gaps remain in our understanding of how thermal stress and bleaching affect the metabolic networks that underpin holobiont function. We applied gas chromatography–mass spectrometry (GC–MS) metabolomics to detect changes in the intracellular free metabolite pools (polar and semi-polar compounds) of in hospite dinoflagellate symbionts and their coral hosts (and any associated microorganisms) during early- and late-stage thermal bleaching (a reduction of approximately 50 and 70% in symbiont density, respectively). We detected characteristic changes to the metabolite profiles of each symbiotic partner associated with individual cellular responses to thermal, oxidative and osmotic stress, which progressed with the severity of bleaching. Alterations were also indicative of changes to energy-generating and biosynthesis pathways in both partners, with a shift to the increased catabolism of lipid stores. Specifically, in symbiont intracellular metabolite pools, we observed accumulations of multiple free fatty acids, plus the chloroplast-associated antioxidant alpha-tocopherol. In the host, we detected a decline in the abundance of pools of multiple carbohydrates, amino acids and intermediates, in addition to the antioxidant ascorbate. These findings further our understanding of the metabolic changes that occur to symbiont and host (and its associated microorganisms) during thermal bleaching. These findings also provide further insight into the largely undescribed roles of free metabolite pools in cellular homeostasis, signalling and acclimation to thermal stress in the cnidarian–dinoflagellate symbiosis.

The ability of corals and other cnidarians to survive climate change depends partly on the composition of their endosymbiont communities. The dinoflagellate family Symbiodiniaceae is genetically and physiologically diverse, and one proposed mechanism for cnidarians to acclimate to rising temperatures is to acquire more thermally tolerant symbionts. However, cnidarian-dinoflagellate associations vary in their degree of specificity, which may limit their capacity to alter symbiont communities. Here, we inoculated symbiont-free polyps of the sea anemone Exaiptasia pallida (commonly referred to as ‘Aiptasia’), a model system for the cnidarian-dinoflagellate symbiosis, with simultaneous or sequential mixtures of thermally tolerant and thermally sensitive species of Symbiodiniaceae. We then monitored symbiont success (relative proportional abundance) at normal and elevated temperatures across two to four weeks. All anemones showed signs of bleaching at high temperature. During simultaneous inoculations, the native, thermally sensitive Breviolum minutum colonized polyps most successfully regardless of temperature when paired against the non-native but more thermally tolerant Symbiodinium microadriaticum or Durusdinium trenchii . Furthermore, anemones initially colonized with B. minutum and subsequently exposed to S. microadriaticum failed to acquire the new symbiont. These results highlight how partner specificity may place strong limitations on the ability of certain cnidarians to acquire more thermally tolerant symbionts, and hence their adaptive potential under climate change.

The genus Symbiodinium is physiologically diverse and so may differentially influence symbiosis establishment and function. To explore this, we inoculated aposymbiotic individuals of the sea anemone Exaiptasia pallida (commonly referred to as “Aiptasia”), a model for coral symbiosis, with one of five Symbiodinium species or types (S. microadriaticum, S. minutum, phylotype C3, S. trenchii, or S. voratum). The spatial pattern of colonization was monitored over time via confocal microscopy, and various physiological parameters were measured to assess symbiosis functionality. Anemones rapidly formed a symbiosis with the homologous symbiont, S. minutum, but struggled or failed to form a long-lasting symbiosis with Symbiodinium C3 or S. voratum, respectively. Symbiodinium microadriaticum and S. trenchii were successful but reached their peak density two weeks after S. minutum. The spatial pattern of colonization was identical for all Symbiodinium taxa that were ultimately successful, starting in the oral disk and progressing to the tentacles, before invading the column and, finally, the pedal disk. In all cases, proliferation through the anemone’s tentacles was patchy, suggesting that symbionts were being expelled into the gastrovascular cavity and re-phagocytosed by the host. However, the timing of these various spatial events differed between the different Symbiodinium taxa. Furthermore, S. microadriaticum and S. trenchii were less beneficial to the host, as indicated by lower rates of photosynthesis, anemone growth, and pedal laceration. This study enhances our understanding of the link between symbiont identity and the performance of the overall symbiosis, which is important for understanding the potential establishment and persistence of novel host-symbiont pairings. Importantly, we also provide a baseline for further studies on this topic with the globally adopted “Aiptasia” model system.

To persist in oligotrophic waters, reef-building corals rely on nutritional interactions with symbiotic dinoflagellates of the family Symbiodiniaceae, but the true diversity of this family remains poorly characterised. In this paper, we assess Symbiodiniaceae richness at Atauro Island (Timor-Leste) as well as on reefs of the neighbouring Timor mainland, using direct sequencing of three gene regions: cob gene, mitochondrion; ITS2 region, nucleus; and psbAncr region, chloroplast; in addition to a highly multiplexed application of next-generation sequencing. These geographic sites are among the most biodiverse in the world, but have never had their symbiont communities studied. Despite their proximity, our results reveal symbiont richness 1.25 times higher at Atauro Island than the Timor mainland, a result evident in dominant sequences. In contrast, Timor had a significantly richer background sequence diversity. Although sampling was restricted to shallow sites only, symbiont richness at Atauro Island was also higher than comparative reefscapes globally, after standardising for number of taxa sampled. While Atauro and Timor have related symbiont populations, with the same novel types recorded at both sites, there were also clear differences in symbiont composition between the two geographic regions, with Timor displaying a consortium more characteristic of stressed reef environments (proportionally hosting twice as many Durusdinium sequences, formerly clade D, as Atauro). These results reveal a symbiont richness that matches the high biodiversity of these reefs, but also potentially negative effects of proximal human populations on Symbiodiniaceae, even when previous studies have shown corals to be largely unaffected.

Within microeukaryotes, genetic variation and functional variation sometimes accumulate more quickly than morphological differences. To understand the evolutionary history and ecology of such lineages, it is key to examine diversity at multiple levels of organization. In the dinoflagellate family Symbiodiniaceae, which can form endosymbioses with cnidarians ( e.g ., corals, octocorals, sea anemones, jellyfish), other marine invertebrates ( e.g. , sponges, molluscs, flatworms), and protists ( e.g ., foraminifera), molecular data have been used extensively over the past three decades to describe phenotypes and to make evolutionary and ecological inferences. Despite advances in Symbiodiniaceae genomics, a lack of consensus among researchers with respect to interpreting genetic data has slowed progress in the field and acted as a barrier to reconciling observations. Here, we identify key challenges regarding the assessment and interpretation of Symbiodiniaceae genetic diversity across three levels: species, populations, and communities. We summarize areas of agreement and highlight techniques and approaches that are broadly accepted. In areas where debate remains, we identify unresolved issues and discuss technologies and approaches that can help to fill knowledge gaps related to genetic and phenotypic diversity. We also discuss ways to stimulate progress, in particular by fostering a more inclusive and collaborative research community. We hope that this perspective will inspire and accelerate coral reef science by serving as a resource to those designing experiments, publishing research, and applying for funding related to Symbiodiniaceae and their symbiotic partnerships.

Some reef corals form stable, dominant or codominant associations with multiple endosymbiotic dinoflagellate species (family Symbiodiniaceae). Given the immense genetic and physiological diversity within this family, Symbiodiniaceae community composition has the potential to impact the nutritional physiology and fitness of the cnidarian host and all associated symbionts. Here we assessed the impact of the symbiont community composition on the metabolome of the coral Montipora capitata in Kāne‘ohe Bay, Hawai‘i, where different colonies can be dominated by stress-tolerant Durusdinium glynnii or stress-sensitive Cladocopium spp. Based on our existing knowledge of these symbiont taxa, we hypothesised that the metabolite profile of D. glynnii-dominated corals would be consistent with poorer nutritional support of the host relative to those corals dominated by Cladocopium spp. However, comparative metabolite profiling revealed that the metabolite pools of the host and symbiont were unaffected by differences in the abundance of the two symbionts within the community. The abundance of the individual metabolites was the same in the host and in the endosymbiont regardless of whether the host was populated with D. glynnii or Cladocopium spp. These results suggest that coral-dinoflagellate symbioses have the potential to undergo physiological adjustments over time to accommodate differences in their resident symbionts. Such mechanisms may involve host heterotrophic compensation (increasing the level of nutrition generated by feeding relative to delivery from the algae), dynamic regulation of metabolic pathways when exchange of metabolites between the organisms differs, and/or modification of both the type and quantity of metabolites that are exchanged. We discuss these adjustments and the implications for the physiology and survival of reef corals under changing environmental regimes.