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As coral reefs struggle to survive under climate change, it is crucial to know whether they have the capacity to withstand changing conditions, particularly increasing seawater temperatures. Thermal tolerance requires the integrative response of the different components of the coral holobiont (coral host, algal photosymbiont, and associated microbiome). Here, using a controlled thermal stress experiment across three divergent Caribbean coral species, we attempt to dissect holobiont member metatranscriptome responses from coral taxa with different sensitivities to heat stress and use phylogenetic ANOVA to study the evolution of gene expression adaptation. We show that coral response to heat stress is a complex trait derived from multiple interactions among holobiont members. We identify host and photosymbiont genes that exhibit lineage-specific expression level adaptation and uncover potential roles for bacterial associates in supplementing the metabolic needs of the coral-photosymbiont duo during heat stress. Our results stress the importance of integrative and comparative approaches across a wide range of species to better understand coral survival under the predicted rise in sea surface temperatures. As corals struggle to survive under climate change, it is crucial to know whether they can withstand increasing seawater temperatures. Using a controlled thermal stress experiment across three divergent coral holobionts, this study examines metatranscriptomic responses to heat stress corresponding to the coral host, photosymbionts and associated microbiota.

The biodiversity in coral reef ecosystems is distributed heterogeneously across spatial and temporal scales, being commonly influenced by biogeographic factors, habitat area and disturbance frequency. A potential association between gradients of usable energy and biodiversity patterns has received little empirical support in these ecosystems. Here, we analyzed the productivity and biodiversity variation over depth gradients in symbiotic coral communities, whose members rely on the energy translocated by photosynthetic algal symbionts (zooxanthellae). Using a mechanistic model we explored the association between the depth-dependent variation in photosynthetic usable energy to corals and gradients of species diversity, comparing reefs with contrasting water clarity and biodiversity patterns across global hotspots of marine biodiversity. The productivity-biodiversity model explained between 64 and 95% of the depth-related variation in coral species richness, indicating that much of the variation in species richness with depth is driven by changes in the fractional contribution of photosynthetically fixed energy by the zooxanthellae. These results suggest a fundamental role of solar energy availability and photosynthetic production in explaining global-scale patterns of coral biodiversity and community structure along depth gradients. Accordingly, the maintenance of water optical quality in coral reefs is fundamental to protect coral biodiversity and prevent reef degradation.

Mass coral bleaching compromises the long-term persistence of coral reefs, yet our current understanding of the different cellular mechanisms leading to the development of a bleached coral is still limited. In this perspective, we mapped the cascade of cellular events and physiological responses of symbiotic corals triggered by thermal stress. Based on existing knowledge, we created an integrated model that describes phenotypic changes induced by sensing mechanisms. Cellular responses are mapped in the context of reactive oxygen species (ROS) production in the algal symbiont chloroplast, followed by signaling to the nucleus and subsequent “leak” to the coral host cell. The starting point is set by ROS production and signaling, which is a day-to-day mechanism by which symbiotic corals maintain homeostasis and acclimate to environmental variation. As stress and acclimation are intimately linked, our model maps coral responses from the initial stimulus in the chloroplast to the complex cascade of events leading to seasonal phenotypic changes ( i.e. , seasonal acclimation), and if stress progresses, to the downstream coral bleached phenotype ( i.e. , when the coral’s capacity to acclimate is overwhelmed by heat stress). Placing acclimation, heat stress and bleaching responses in a common ground is a critical step to reduce the source of uncertainty in understanding the coral response to climate change, fundamental for the development of predictive climate models.

Degradation of water optical properties due to anthropogenic disturbances is a common phenomenon in coastal waters globally. Although this condition is associated with multiple drivers that affect corals health in multiple ways, its effect on light availability and photosynthetic energy acquisition has been largely neglected. Here, we describe how declining the water optical quality in a coastal reef exposed to a turbid plume of water originating from a man-made channel compromises the functionality of the keystone coral species Orbicella faveolata. We found highly variable water optical conditions with significant effects on the light quantity and quality available for corals. Low-light phenotypes close to theoretical limits of photoacclimation were found at shallow depths as a result of reduced light penetration. The estimated photosynthetically fixed energy depletion with increasing depth was associated with patterns of colony mortality and vertical habitat compression. A numerical model illustrates the potential effect of the progressive water quality degradation on coral mortality and population decline along the depth gradient. Collectively, our findings suggest that preserving the water properties seeking to maximize light penetration through the water column is essential for maintaining the coral reef structure and associated ecosystem services.

Coral reefs are undergoing degradation due to overexploitation, pollution, and climate change. Management and restoration efforts require that we gain a better understanding of the complex interactions between corals, their microbiomes, and their environment. For this purpose, Varadero Reef near Cartagena, Colombia, serves as an informative study system located at the entrance of the Bay of Cartagena adjacent to the Canal del Dique, which carries turbid and polluted water into the bay. Varadero’s survival under poor environmental conditions makes it a great study site for investigating the relationship between the microbiome and coral resistance to environmental stressors. To determine whether the microbiomes of Varadero corals differ from those in less impacted sites, we conducted a reciprocal transplant experiment by relocating coral fragments from Varadero as well as a geographically proximate reef that is less affected by plume dynamics (Rosario) across a gradient of turbidity (low, medium, and high). After 6 months of acclimatization, transplanted corals developed site-specific microbiomes that differed significantly from pre-transplant microbiomes, and corals transplanted to the highly impacted site from both Varadero and Rosario site saw higher mortality and an increase in overall microbial diversity. In combination with physiology and survivorship outcomes pointing to a limit in the corals’ photoacclimative capacity, our results indicate that, rather than surviving, Varadero Reef is experiencing a slow decline, and its corals are likely on the brink of dysbiosis. With continued anthropogenic interference in marine environments, sites such as Varadero will become increasingly common, and it is imperative that we understand how corals and their microbial symbionts are changing in response to these new environmental conditions.

Many cnidarians host single-celled algae within gastrodermal cells, yielding a mutually beneficial exchange of nutrients between host and symbiont, and dysbiosis can lead to host mortality. Previous research has uncovered symbiosis tradeoffs, including suppression of immune pathways in hosts, and correlations between symbiotic state and pathogen susceptibility. Here, we used a multiomic approach to characterize symbiotic states of the facultatively symbiotic coral Oculina arbuscula by generating genotype-controlled fragments of symbiotic and aposymbiotic tissue. 16S rRNA gene sequencing showed no difference in bacterial communities between symbiotic states. Whole-organism proteomics revealed differential abundance of proteins related to immunity, confirming immune suppression during symbiosis. Single-cell RNAseq identified diverse cell clusters within seven cell types across symbiotic states. Specifically, the gastrodermal cell clusters containing algal-hosting cells from symbiotic tissue had higher expression of nitrogen cycling and lipid metabolism genes than aposymbiotic gastrodermal cells. Furthermore, differential enrichment of immune system gene pathways and lower expression of genes involved in immune regulation were observed in these gastrodermal cells from symbiotic tissue. However, there were no differences in gene expression in the immune cell cluster between symbiotic states. We conclude that there is evidence for compartmentalization of immune system regulation in specific gastrodermal cells in symbiosis. This compartmentalization may limit symbiosis tradeoffs by dampening immunity in algal-hosting cells while simultaneously maintaining general organismal immunity.

Coral reefs are beginning to experience conditions unlike any in recent history. Understanding ecosystem function on future reefs will require reassessing ecological processes under novel environmental regimes. For many coastal reefs, severely degraded water quality will be a hallmark of these novel regimes. While herbivory has traditionally been considered essential for maintaining coral dominance, recent evidence from urban reefs suggests this pattern may be changing. Here, we reexamined the impacts of herbivores on a shallow, turbid reef exposed to extensive coastal development. We found that although herbivore biomass, size-structure, and grazing rates were significantly reduced relative to a nearby protected reef, coral cover on this shallow urban reef remained > 45%. In contrast, coral cover at the nearby protected site was roughly 50% lower. Differences in coral cover between the sites were due to greater cover of two groups of corals at the urban site: depth-generalist Orbicella spp., particularly O. faveolata, and Agaricia spp. with weedy life-history characteristics. Both groups are tolerant of low light but susceptible to coral bleaching. Our results suggest that diminished top-down pressure did not promote algal dominance. Instead, turbidity-induced reductions in available light drove community structure, leading to dominance of coral and algae species able to acclimate to low-light. Our study demonstrates how environmental context can alter the importance of critical processes on coral reefs and highlights the need to reexamine traditional paradigms in reef ecology to understand ecosystem function on future reefs.

Abstract Degradation of water optical properties due to anthropogenic disturbances is a common phenomenon in coastal waters globally. Although this condition is associated with multiple drivers that affect corals health in multiple ways, its effect on light availability and photosynthetic energy acquisition has been largely neglected. Here, we describe how declining the water optical quality in a coastal reef exposed to a turbid plume of water originating from a man-made channel compromise the functionality of the keystone coral species Orbicella faveolata. We found highly variable water optical conditions with significant effects on the light quantity and quality available for corals. Reduction of light penetration into the water column elicits the development of low-light phenotypes close to theoretical limits of photoacclimation despite their occurrence at shallow depths. Predicted photosynthetic energy depletion with increasing depth is associated with patterns of colony mortality and contraction of the habitable space for the population. A numerical model illustrates the potential effect the progressive degradation of water optical properties on the gradual mortality and population decline of O. faveolata. Our findings suggest that preserving the water optical properties seeking to maximize light penetration into the water column may have an extraordinary impact on coral reefs conservation, mostly toward the deeper portions of reefs. Competing Interest Statement The authors have declared no competing interest. Footnotes * https://figshare.com/s/e5e49575f67b90202579

Many cnidarians host single-celled algae within gastrodermal cells, yielding a mutually beneficial exchange of nutrients between host and symbiont, and dysbiosis can lead to host mortality. Previous research has uncovered symbiosis tradeoffs, including suppression of immune pathways in cnidarians hosting intracellular algae and correlations between symbiotic state and pathogen susceptibility. Here, we used a multiomic approach to characterize symbiotic states of the facultatively symbiotic coral Oculina arbuscula by generating genotype-controlled fragments of symbiotic and aposymbiotic tissue. 16S metabarcoding showed no difference in bacterial communities between symbiotic states. Whole-organism proteomics revealed differential abundance of proteins related to immunity, confirming immune suppression during symbiosis. Finally, single-cell RNAseq identified diverse cell clusters within seven cell types across symbiotic states. Specifically, the gastrodermal cell clusters containing algal-hosting cells from symbiotic tissue had higher expression of nitrogen cycling and sugar transport genes than aposymbiotic gastrodermal cells. Furthermore, differential enrichment of immune system gene pathways and lower expression of genes involved in immune regulation were observed in these gastrodermal cells from symbiotic tissue. However, no differences in immune gene expression in the immune cell cluster were observed between symbiotic states. This work reveals a compartmentalization of immune system regulation in specific gastrodermal cells in symbiosis, which may limit symbiosis tradeoffs by simultaneously dampening immunity in algal-hosting cells while maintaining general organismal immunity.Competing Interest StatementThe authors have declared no competing interest.Footnotes* 1) We have performed a thorough bioinformatic comparison of mapping efficiency and quality control metrics of our single-cell data to two new references (a previously published transcriptome of the host coral Oculina arbuscula and a de novo assembled transcriptome from our single cell data) and concluded that the original Astrangia poculata genome provided higher quality mapping, as confirmed by several metrics. 2) We have conducted additional analyses to more confidently identify the cells hosting algal symbionts by analyzing reads mapping to the algal transcriptome. We have added further analysis demonstrating shared cell trajectories of symbiotic O. arbuscula gastrodermal cells to support our conclusions of algal-hosting cell identity. 3) We have included comparative analyses of gastrodermal algal-hosting cells from a previously published paper in the soft coral Xenia sp using orthologous genes. 4) We have provided additional methodological details and quality control testing in the main manuscript as well as additional supplemental figures and datasets. 5) We have included supplemental materials highlighting more in-depth analysis of all cell clusters identified in the manuscript. 6) We toned down some of the language around immune system compartmentalization while simultaneously bolstering our findings with additional analyses. We changed the title of the manuscript to reflect these changes 7) We have published a protocols.io methodology (DOI will be available pending manuscript acceptance) detailing the sample preparation and cell isolation.

Climate change has caused drastic declines in corals. As sessile organisms, response to shifting environmental conditions may include changes in gene expression, epigenetic modifications, or the microbiome, but as of yet, a common mechanism of stress response, alternative splicing (AS), has been under-explored in corals. Using short-term acute thermal stress assays, we investigated patterns of AS in the scleractinian coral Acropora cervicornis during response to and a subsequent overnight recovery phase from low (33°C), medium (35°C), and high (37°C) levels of heat stress. We find that 40 percent of the genomic gene set is subject to AS. Our findings demonstrate conserved and dynamic shifts in splicing profiles during the heat treatment and subsequent recovery phase. AS increased in response to heat stress and was primarily dominated by intron retention in specific classes of transcripts, including those related to splicing regulation itself. While AS returned to baseline levels post-exposure to low heat, AS persisted even after reprieve from higher levels of heat stress. Partial overlap of AS transcripts with differentially expressed genes suggests that AS may represent a distinct and previously under-appreciated regulatory mechanism for thermal stress response in corals.