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A coral reef genome Coral reefs are among the most biologically diverse ecosystems on the planet and are of great economic importance. They are under threat because the scleractinian corals at their core are susceptible to ocean acidification and rising seawater temperatures. The genome of the reef-building coral Acropora digitifera has been analysed with a view to understanding the molecular basis of symbiosis and responses to environmental change. The coral seems to have lost a key enzyme of cysteine biosynthesis, so may be dependent on its symbionts for this amino acid. It contains several genes with roles in protection from ultraviolet light that may have been acquired by horizontal transfer from prokaryotic organisms. The coral's innate immunity repertoire is more complex than that of the solitary sea anemone, suggesting that some of these genes are involved in symbiosis or coloniality. Despite the enormous ecological and economic importance of coral reefs, the keystone organisms in their establishment, the scleractinian corals, increasingly face a range of anthropogenic challenges including ocean acidification and seawater temperature rise 1 , 2 , 3 , 4 . To understand better the molecular mechanisms underlying coral biology, here we decoded the approximately 420-megabase genome of Acropora digitifera using next-generation sequencing technology. This genome contains approximately 23,700 gene models. Molecular phylogenetics indicate that the coral and the sea anemone Nematostella vectensis diverged approximately 500 million years ago, considerably earlier than the time over which modern corals are represented in the fossil record (∼240 million years ago) 5 . Despite the long evolutionary history of the endosymbiosis, no evidence was found for horizontal transfer of genes from symbiont to host. However, unlike several other corals, Acropora seems to lack an enzyme essential for cysteine biosynthesis, implying dependency of this coral on its symbionts for this amino acid. Corals inhabit environments where they are frequently exposed to high levels of solar radiation, and analysis of the Acropora genome data indicates that the coral host can independently carry out de novo synthesis of mycosporine-like amino acids, which are potent ultraviolet-protective compounds. In addition, the coral innate immunity repertoire is notably more complex than that of the sea anemone, indicating that some of these genes may have roles in symbiosis or coloniality. A number of genes with putative roles in calcification were identified, and several of these are restricted to corals. The coral genome provides a platform for understanding the molecular basis of symbiosis and responses to environmental changes.

One of the most conserved traits in the evolution of biomineralizing organisms is the taxon-specific selection of skeletal minerals. All modern scleractinian corals are thought to produce skeletons exclusively of the calcium-carbonate polymorph aragonite. Despite strong fluctuations in ocean chemistry (notably the Mg/Ca ratio), this feature is believed to be conserved throughout the coral fossil record, spanning more than 240 million years. Only one example, the Cretaceous scleractinian coral Coelosmilia (ca. 70 to 65 Ma), is thought to have produced a calcitic skeleton. Here, we report that the modern asymbiotic scleractinian coral Paraconotrochus antarcticus living in the Southern Ocean forms a two-component carbonate skeleton, with an inner structure made of high-Mg calcite and an outer structure composed of aragonite. P. antarcticus and Cretaceous Coelosmilia skeletons share a unique microstructure indicating a close phylogenetic relationship, consistent with the early divergence of P. antarcticus within the Vacatina (i.e., Robusta) clade, estimated to have occurred in the Mesozoic (ca. 116 Mya). Scleractinian corals thus join the group of marine organisms capable of forming bimineralic structures, which requires a highly controlled biomineralization mechanism; this capability dates back at least 100 My. Due to its relatively prolonged isolation, the Southern Ocean stands out as a repository for extant marine organisms with ancient traits.

Little is known about how stony corals build their calcareous skeletons. There are two prevailing hypotheses: that it is a physicochemically dominated process and that it is a biologically mediated one. Using a combination of ultrahigh-resolution three-dimensional imaging and two-dimensional solid-state nuclear magnetic resonance (NMR) spectroscopy, we show that mineral deposition is biologically driven. Randomly arranged, amorphous nanoparticles are initially deposited in microenvironments enriched in organic material; they then aggregate and form ordered aragonitic structures through crystal growth by particle attachment. Our NMR results are consistent with heterogeneous nucleation of the solid mineral phase driven by coral acid-rich proteins. Such a mechanism suggests that stony corals may be able to sustain calcification even under lower pH conditions that do not favor the inorganic precipitation of aragonite.

Corals from the northern Red Sea and Gulf of Aqaba exhibit extreme thermal tolerance. To examine the underlying gene expression dynamics, we exposed Stylophora pistillata from the Gulf of Aqaba to short-term (hours) and long-term (weeks) heat stress with peak seawater temperatures ranging from their maximum monthly mean of 27 °C (baseline) to 29.5 °C, 32 °C, and 34.5 °C. Corals were sampled at the end of the heat stress as well as after a recovery period at baseline temperature. Changes in coral host and symbiotic algal gene expression were determined via RNA-sequencing (RNA-Seq). Shifts in coral microbiome composition were detected by complementary DNA (cDNA)-based 16S ribosomal RNA (rRNA) gene sequencing. In all experiments up to 32 °C, RNA-Seq revealed fast and pervasive changes in gene expression, primarily in the coral host, followed by a return to baseline gene expression for the majority of coral (>94%) and algal (>71%) genes during recovery. At 34.5 °C, large differences in gene expression were observed with minimal recovery, high coral mortality, and a microbiome dominated by opportunistic bacteria (including Vibrio species), indicating that a lethal temperature threshold had been crossed. Our results show that the S. pistillata holobiont can mount a rapid and pervasive gene expression response contingent on the amplitude and duration of the thermal stress. We propose that the transcriptomic resilience and transcriptomic acclimation observed are key to the extraordinary thermal tolerance of this holobiont and, by inference, of other northern Red Sea coral holobionts, up to seawater temperatures of at least 32 °C, that is, 5 °C above their current maximum monthly mean

Transcriptome and genome data from twenty stony coral species and a selection of reference bilaterians were studied to elucidate coral evolutionary history. We identified genes that encode the proteins responsible for the precipitation and aggregation of the aragonite skeleton on which the organisms live, and revealed a network of environmental sensors that coordinate responses of the host animals to temperature, light, and pH. Furthermore, we describe a variety of stress-related pathways, including apoptotic pathways that allow the host animals to detoxify reactive oxygen and nitrogen species that are generated by their intracellular photosynthetic symbionts, and determine the fate of corals under environmental stress. Some of these genes arose through horizontal gene transfer and comprise at least 0.2% of the animal gene inventory. Our analysis elucidates the evolutionary strategies that have allowed symbiotic corals to adapt and thrive for hundreds of millions of years. For millions of years, reef-building stony corals have created extensive habitats for numerous marine plants and animals in shallow tropical seas. Stony corals consist of many small, tentacled animals called polyps. These polyps secrete a mineral called aragonite to create the reef – an external ‘skeleton’ that supports and protects the corals. Photosynthesizing algae live inside the cells of stony corals, and each species depends on the other to survive. The algae produce the coral’s main source of food, although they also produce some waste products that can harm the coral if they build up inside cells. If the oceans become warmer and more acidic, the coral are more likely to become stressed and expel the algae from their cells in a process known as coral bleaching. This makes the coral more likely to die or become diseased. Corals have survived previous periods of ocean warming, although it is not known how they evolved to do so. The evolutionary history of an organism can be traced by studying its genome – its complete set of DNA – and the RNA molecules encoded by these genes. Bhattacharya et al. performed this analysis for twenty stony coral species, and compared the resulting genome and RNA sequences with the genomes of other related marine organisms, such as sea anemones and sponges. In particular, Bhattacharya et al. examined “ortholog” groups of genes, which are present in different species and evolved from a common ancestral gene. This analysis identified the genes in the corals that encode the proteins responsible for constructing the aragonite skeleton. The coral genome also encodes a network of environmental sensors that coordinate how the polyps respond to temperature, light and acidity. Bhattacharya et al. also uncovered a variety of stress-related pathways, including those that detoxify the polyps of the damaging molecules generated by algae, and the pathways that enable the polyps to adapt to environmental stress. Many of these genes were recruited from other species in a process known as horizontal gene transfer. The oceans are expected to become warmer and more acidic in the coming centuries. Provided that humans do not physically destroy the corals’ habitats, the evidence found by Bhattacharya et al. suggests that the genome of the corals contains the diversity that will allow them to adapt to these new conditions.

Viruses, microbes, and host macroorganisms form ecological units called holobionts. Here, a combination of metagenomic sequencing, metabolomic profiling, and epifluorescence microscopy was used to investigate how the different components of the holobiont including bacteria, viruses, and their associated metabolites mediate ecological interactions between corals and turf algae. The data demonstrate that there was a microbial assemblage unique to the coral-turf algae interface displaying higher microbial abundances and larger microbial cells. This was consistent with previous studies showing that turf algae exudates feed interface and coral-associated microbial communities, often at the detriment of the coral. Further supporting this hypothesis, when the metabolites were assigned a nominal oxidation state of carbon (NOSC), we found that the turf algal metabolites were significantly more reduced (i.e., have higher potential energy) compared to the corals and interfaces. The algae feeding hypothesis was further supported when the ecological outcomes of interactions (e.g., whether coral was winning or losing) were considered. For example, coral holobionts losing the competition with turf algae had higher Bacteroidetes-to-Firmicutes ratios and an elevated abundance of genes involved in bacterial growth and division. These changes were similar to trends observed in the obese human gut microbiome, where overfeeding of the microbiome creates a dysbiosis detrimental to the long-term health of the metazoan host. Together these results show that there are specific biogeochemical changes at coral–turf algal interfaces that predict the competitive outcomes between holobionts and are consistent with algal exudates feeding coral-associated microbes.

Many corals harbour symbiotic dinoflagellate algae. The algae live inside coral cells in a specialized membrane compartment known as the symbiosome, which shares the photosynthetically fixed carbon with coral host cells while host cells provide inorganic carbon to the algae for photosynthesis 1 . This endosymbiosis—which is critical for the maintenance of coral reef ecosystems—is increasingly threatened by environmental stressors that lead to coral bleaching (that is, the disruption of endosymbiosis), which in turn leads to coral death and the degradation of marine ecosystems 2 . The molecular pathways that orchestrate the recognition, uptake and maintenance of algae in coral cells remain poorly understood. Here we report the chromosome-level genome assembly of a Xenia species of fast-growing soft coral 3 , and use this species as a model to investigate coral–alga endosymbiosis. Single-cell RNA sequencing identified 16 cell clusters, including gastrodermal cells and cnidocytes, in Xenia sp. We identified the endosymbiotic cell type, which expresses a distinct set of genes that are implicated in the recognition, phagocytosis and/or endocytosis, and maintenance of algae, as well as in the immune modulation of host coral cells. By coupling Xenia sp. regeneration and single-cell RNA sequencing, we observed a dynamic lineage progression of the endosymbiotic cells. The conserved genes associated with endosymbiosis that are reported here may help to reveal common principles by which different corals take up or lose their endosymbionts. Single-cell RNA sequencing identifies the pattern of gene expression during lineage progression in endosymbiotic cells of the fast-growing soft coral Xenia , revealing principles that underlie uptake and maintenance of endosymbionts by this coral.

Insight into the response of reef corals and other major marine calcifiers to ocean acidification is limited by a lack of knowledge about how seawater pH and carbonate chemistry impact the physiological processes that drive biomineralization. Ocean acidification is proposed to reduce calcification rates in corals by causing declines in internal pH at the calcifying tissue-skeleton interface where biomineralization takes place. Here, we performed an in vivo study on how partial-pressure CO₂-driven seawater acidification impacts intracellular pH in coral calcifying cells and extracellular pH in the fluid at the tissue-skeleton interface [subcalicoblastic medium (SCM)] in the coral Stylophora pistil lata. We also measured calcification in corals grown under the same conditions of seawater acidification by measuring lateral growth of colonies and growth of aragonite crystals under the calcifying tissue. Our findings confirm that seawater acidification decreases pH of the SCM, but this decrease is gradual relative to the surrounding seawater, leading to an increasing pH gradient between the SCM and seawater. Reductions in calcification rate, both at the level of crystals and whole colonies, were only observed in our lowest pH treatment when pH was significantly depressed in the calcifying cells in addition to the SCM. Overall, our findings suggest that reef corals may mitigate the effects of seawater acidification by regulating pH in the SCM, but they also highlight the role of calcifying cell pH homeostasis in determining the response of reef corals to changes in external seawater pH and carbonate chemistry.

Abstract Corals live in a complex, multipartite symbiosis with diverse microbes across kingdoms, some of which are implicated in vital functions, such as those related to resilience against climate change. However, knowledge gaps and technical challenges limit our understanding of the nature and functional significance of complex symbiotic relationships within corals. Here, we provide an overview of the complexity of the coral microbiome focusing on taxonomic diversity and functions of well-studied and cryptic microbes. Mining the coral literature indicate that while corals collectively harbour a third of all marine bacterial phyla, known bacterial symbionts and antagonists of corals represent a minute fraction of this diversity and that these taxa cluster into select genera, suggesting selective evolutionary mechanisms enabled these bacteria to gain a niche within the holobiont. Recent advances in coral microbiome research aimed at leveraging microbiome manipulation to increase coral’s fitness to help mitigate heat stress-related mortality are discussed. Then, insights into the potential mechanisms through which microbiota can communicate with and modify host responses are examined by describing known recognition patterns, potential microbially derived coral epigenome effector proteins and coral gene regulation. Finally, the power of omics tools used to study corals are highlighted with emphasis on an integrated host–microbiota multiomics framework to understand the underlying mechanisms during symbiosis and climate change-driven dysbiosis. Corals live in intimate relationships with an intricate collection of microbes that are crucial for their functioning; therefore, understanding the molecular basis of the interactions of the coral host and its associated microbiome is vital for coral resilience in a warming ocean.

Determining the adaptive potential of foundation species, such as reef-building corals, is urgent as the oceans warm and coral populations decline. Theory predicts that corals may adapt to climate change via selection on standing genetic variation. Yet, corals face not only rising temperatures but also novel diseases. We studied the interaction between two major stressors affecting colonies of the threatened coral, Acropora cervicornis: white-band disease and high water temperature. We determined that 27% of A. cervicornis were disease resistant prior to a thermal anomaly. However, disease resistance was largely lost during a bleaching event because of more compromised coral hosts or increased pathogenic dose/virulence. There was no tradeoff between disease resistance and temperature tolerance; disease susceptibility was independent of Symbiodinium strain. The present study shows that susceptibility to temperature stress creates an increased risk in disease-associated mortality, and only rare genets may maintain or gain infectious disease resistance under high temperature. We conclude that A. cervicornis populations in the lower Florida Keys harbor few existing genotypes that are resistant to both warming and disease. The staghorn coral was once prevalent throughout the Florida Reef Tract. However, the last few decades have seen a substantial reduction in the coral population because of disease outbreaks and increasing ocean temperatures. The staghorn coral shows no evidence of natural recovery, and so has been the focus of restoration efforts throughout much of the Florida region. Why put the time and effort into growing corals that are unlikely to survive within environmental conditions that continue to deteriorate? One reason is that the genetic make-up – the genotype – of some corals makes them more resilient to certain threats. However, there could be tradeoffs associated with these resilient traits. For example, a coral may be able to tolerate heat, but may easily succumb to disease. Previous studies have identified some staghorn coral genotypes that are resistant to an infection called white-band disease. The influence of high water temperatures on the ability of the coral to resist this disease was not known. There also remained the possibility that more varieties of coral might show similar disease resistance. To investigate Muller et al. conducted two experiments exposing staghorn coral genotypes to white-band diseased tissue before and during a coral bleaching event. Approximately 25% of the population of staghorn tested was resistant to white-band disease before the bleaching event. When the corals were exposed to white-band disease during bleaching, twice as much of the coral died. Two out of the 15, or 13%, of the coral genotypes tested were resistant to the disease even while bleached. Additionally, the level of bleaching within the coral genotypes was not related to how easily they developed white-band disease, suggesting that there are no direct tradeoffs between heat tolerance and disease resistance. These results suggest that there are very hardy corals, created by nature, already in existence. Incorporating these traits thoughtfully into coral restoration plans may increase the likelihood of population-based recovery. The Florida Reef Tract is estimated to be worth over six billion dollars to the state economy, providing over 70,000 jobs and attracting millions of tourists into Florida each year. However, much of these ecosystem services will be lost if living coral is not restored within the reef tract. The results presented by Muller et al. emphasize the need for maintaining high genetic diversity while increasing resiliency when restoring coral. They also emphasize that disease resistant corals, even when bleached, already exist and may be an integral part of the recovery of Florida’s reef tract.