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Abstract Reef-building corals are integral ecosystem engineers in tropical coral reefs worldwide but are increasingly threatened by climate change and rising ocean temperatures. Consequently, there is an urgency to identify genetic, epigenetic, and environmental factors, and how they interact, for species acclimatization and adaptation. The availability of genomic resources is essential for understanding the biology of these organisms and informing future research needs for management and and conservation. The highly diverse coral genusAcroporaboasts the largest number of high-quality coral genomes, but these remain limited to a few geographic regions and highly studied species. Here we present the assembly and annotation of the genome and DNA methylome ofAcropora pulchrafrom Mo’orea, French Polynesia. The genome assembly was created from a combination of long-read PacBio HiFi data, from which DNA methylation data were also called and quantified, and additional Illumina RNASeq data forab initiogene predictions. The work presented here resulted in the most completeAcroporagenome to date, with a BUSCO completeness of 96.7% metazoan genes. The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. Structural and functional annotation resulted in the prediction of a total of 40,518 protein-coding genes, and 16.74% of the genome in repeats. DNA methylation in the CpG context was 14.6% and predominantly found in flanking and gene body regions (61.7%). This reference assembly of theA. pulchragenome and DNA methylome will provide the capacity for further mechanistic studies of a common coastal coral in French Polynesia of great relevance for restoration and improve our capacity for comparative genomics inAcroporaand cnidarians more broadly. 

Reef-building corals are integral ecosystem engineers of tropical reefs but face threats from climate change. Investigating genetic, epigenetic, and environmental factors influencing their adaptation is critical. Genomic resources are essential for understanding coral biology and guiding conservation efforts. However, genomes of the coral genus Acropora are limited to highly-studied species. Here, we present the assembly and annotation of the genome and DNA methylome of Acropora pulchra from Mo’orea, French Polynesia. Using long-read PacBio HiFi and Illumina RNASeq, we generated the most complete Acropora genome to date (BUSCO completeness of 96.7% metazoan genes). The assembly size is 518 Mbp, with 174 scaffolds, and a scaffold N50 of 17 Mbp. We predicted 40,518 protein-coding genes and 16.74% of the genome in repeats. DNA methylation in the CpG context is 14.6%. This assembly of the A. pulchra genome and DNA methylome will support studies of coastal corals in French Polynesia, aiding conservation and comparative studies of Acropora and cnidarians. 

Abstract The elkhorn coral,Acropora palmata, was historically a major reef-building species in the Caribbean, but has suffered devastating declines in recent decades. Despite significant restoration efforts in Florida, the marine heatwave of 2023 caused severe bleaching and mortality to both wild and restored colonies. To understand the disastrous impacts, we evaluated the variation in heat tolerance among Florida’sA. palmatapopulation prior to the event. In 2022, we used rapid acute heat stress assays to assess the thermal tolerance of 172 adult colonies (125 unique genets) from four nurseries. We found variation in thermal tolerance (4.17°C range in ED50) that was attributed to nursery location (17.2% of variation), genet (25.9%), and symbiont abundance (15.6%). Algal symbiont type, however, was the strongest predictor of thermal performance, with the few (n = 10) colonies hostingDurusdiniumbeing, on average, 1.9°C more thermally tolerant than corals hostingSymbiodinium. This difference would have decreased the effective heat stress accumulation during the 2023 event by ~92%. Therefore, despite considerable variation in thermal tolerance among Florida’s elkhorn corals, hostingDurusdiniumappears to be the most effective mechanism for surviving such extreme heat stress. These findings suggest that restoration strategies that focus on rearing sexually derivedA. palmatarecruits withDurusdinium, followed by outplanting to suitable environments, may improve survival during future heatwaves. Combined with efforts to introduce additional elkhorn diversity from populations outside Florida, these approaches may be the most effective interventions to promote the continued survival of Florida’s elkhorn corals in the face of rapid climate change. 

Abstract The coral-dinoflagellate endosymbiosis is based on nutrient exchanges that impact holobiont energetics. Of particular concern is the breakdown or dysbiosis of this partnership that is seen in response to elevated temperatures, where loss of symbionts through coral bleaching can lead to starvation and mortality. Here we extend a dynamic bioenergetic model of coral symbioses to explore the mechanisms by which temperature impacts various processes in the symbiosis and to enable simulational analysis of thermal bleaching. Our model tests the effects of two distinct mechanisms for how increased temperature impacts the symbiosis: 1) accelerated metabolic rates due to thermodynamics and 2) damage to the photosynthetic machinery of the symbiont caused by heat stress. Model simulations show that the model can capture key biological responses to different levels of increased temperatures. Moderately increased temperatures increase metabolic rates and slightly decrease photosynthesis. The slightly decreased photosynthesis rates cause the host to receive less carbon and share more nitrogen with the symbiont. This results in temporarily increased symbiont growth and a higher symbiont/host ratio. In contrast, higher temperatures cause a breakdown of the symbiosis due to escalating feedback that involves further reduction in photosynthesis and insufficient energy supply for$$\hbox {CO}_2$$ ${\text{CO}}_2$concentration by the host. This leads to the accumulation of excess light energy and the generation of reactive oxygen species, eventually triggering symbiont expulsion and coral bleaching. Importantly, bleaching does not result from accelerated metabolic rates alone; it only occurs as a result of the photodamage mechanism due to its effect on nutrient cycling. Both higher light intensities and higher levels of DIN render corals more susceptible to heat stress. Conversely, heterotrophic feeding can increase the maximal temperature that can be tolerated by the coral. Collectively these results show that a bioenergetics model can capture many observed patterns of heat stress in corals, such as higher metabolic rates and higher symbiont/host ratios at moderately increased temperatures and symbiont expulsion at strongly increased temperatures. 

Monitoring coral cover can describe the ecology of reef degradation, but rarely can it reveal the proximal mechanisms of change, or achieve its full potential in informing conservation actions. Describing temporal variation in Symbiodiniaceae within corals can help address these limitations, but this is rarely a research priority. Here, we augmented an ecological time series of the coral reefs of St. John, US Virgin Islands, by describing the genetic complement of symbiotic algae in common corals. Seventy-five corals from nine species were marked and sampled in 2017. Of these colonies, 41% were sampled in 2018, and 72% in 2019; 28% could not be found and were assumed to have died. Symbiodiniaceae ITS2 sequencing identified 525 distinct sequences (comprising 42 ITS2 type profiles), and symbiont diversity differed among host species and individuals, but was in most cases preserved within hosts over 3 yrs that were marked by physical disturbances from major hurricanes (2017) and the regional onset of stony coral tissue loss disease (2019). While changes in symbiont communities were slight and stochastic over time within colonies, variation in the dominant symbionts among colonies was observed for all host species. Together, these results indicate that declining host abundances could lead to the loss of rare algal lineages that are found in a low proportion of few coral colonies left on many reefs, especially if coral declines are symbiont-specific. These findings highlight the importance of identifying Symbiodiniaceae as part of a time series of coral communities to support holistic conservation planning. Repeated sampling of tagged corals is unlikely to be viable for this purpose, because many Caribbean corals are dying before they can be sampled multiple times. Instead, random sampling of large numbers of corals may be more effective in capturing the diversity and temporal dynamics of Symbiodiniaceae metacommunities in reef corals. 

In 2023, a record-setting marine heat wave triggered the ninth mass coral bleaching event on Florida’s Coral Reef (FCR). We examined spatial patterns of heat exposure along the ~560-kilometer length of FCR and the mortality of two ecologically important, critically endangered reef-building corals. Sea surface temperatures were ≥31°C for an average of 40.7 days, leading to heat exposures 2.2- to fourfold higher than all prior years on record. In the Florida Keys and Dry Tortugas, 97.8 to 100% of theAcropora palmataandAcropora cervicorniscolonies died. Mortality was lower offshore southeast Florida (37.9%), reflecting cooler temperatures in this region. Since the late 1970s, multiple stressors had already reduced the ecological relevance ofAcroporain Florida, but the 2023 heat wave marks their functional extinction from FCR. 

Some reef-building corals form symbioses with multiple algal partners that differ in ecologically important traits like heat tolerance. Coral bleaching and recovery can drive symbiont community turnover toward more heat-tolerant partners, and this ‘adaptive bleaching’ response can increase future bleaching thresholds by 1–2°C, aiding survival in warming oceans. However, this mechanism of rapid acclimatization only occurs in corals that are compatible with multiple symbionts, and only when the disturbance regime and competitive dynamics among symbionts are sufficient to bring about community turnover. The full scope of coral taxa and ecological scenarios in which symbiont shuffling occurs remains poorly understood, though its prevalence is likely to increase as warming oceans boost the competitive advantage of heat-tolerant symbionts, increase the frequency of bleaching events, and strengthen metacommunity feedbacks. Still, the constraints, limitations, and potential tradeoffs of symbiont shuffling suggest it will not save coral reef ecosystems; however, it may significantly improve the survival trajectories of some, or perhaps many, coral species. Interventions to manipulate coral symbionts and symbiont communities may expand the scope of their adaptive potential, which may boost coral survival until climate change is addressed.