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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. 

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. 

Abstract Dynamic Energy Budget models relate whole organism processes such as growth, reproduction and mortality to suborganismal metabolic processes. Much of their potential derives from extensions of the formalism to describe the exchange of metabolic products between organisms or organs within a single organism, for example the mutualism between corals and their symbionts. Without model simplification, such models are at risk of becoming parameter-rich and hence impractical. One natural simplification is to assume that some metabolic processes act on ‘fast’ timescales relative to others. A common strategy for formulating such models is to assume that ‘fast’ processes equilibrate immediately, while ‘slow’ processes are described by ordinary differential equations. This strategy can bring a subtlety with it. What if there are multiple, interdependent fast processes that have multiple equilibria, so that additional information is needed to unambiguously specify the model dynamics? This situation can easily arise in contexts where an organism or community can persist in a ‘healthy’ or an ‘unhealthy’ state with abrupt transitions between states possible. To approach this issue, we offer the following: (a) a method to unambiguously complete implicitly defined models by adding hypothetical ‘fast’ state variables; (b) an approach for minimizing the number of additional state variables in such models, which can simplify the numerical analysis and give insights into the model dynamics; and (c) some implications of the new approach that are of practical importance for model dynamics, e.g. on the bistability of flux dynamics and the effect of different initialization choices on model outcomes. To demonstrate those principles, we use a simplified model for root-shoot dynamics of plants and a related model for the interactions between corals and endosymbiotic algae that describes coral bleaching and recovery. 

Abstract Algal symbiont shuffling in favour of more thermotolerant species has been shown to enhance coral resistance to heat‐stress. Yet, the mechanistic underpinnings and long‐term implications of these changes are poorly understood. This work studied the modifications in coral DNA methylation, an epigenetic mechanism involved in coral acclimatization, in response to symbiont manipulation and subsequent heat stress exposure. Symbiont composition was manipulated in the great star coralMontastraea cavernosathrough controlled thermal bleaching and recovery, producing paired ramets of three genets dominated by either their native symbionts (genusCladocopium) or the thermotolerant species (Durusdinium trenchi). Single‐base genome‐wide analyses showed significant modifications in DNA methylation concentrated in intergenic regions, introns and transposable elements. Remarkably, DNA methylation changes in response to heat stress were dependent on the dominant symbiont, with twice as many differentially methylated regions found in heat‐stressed corals hosting different symbionts (Cladocopiumvs.D.trenchii) compared to all other comparisons. Interestingly, while differential gene body methylation was not correlated with gene expression, an enrichment in differentially methylated regions was evident in repetitive genome regions. Overall, these results suggest that changes in algal symbionts favouring heat tolerant associations are accompanied by changes in DNA methylation in the coral host. The implications of these results for coral adaptation, along with future avenues of research based on current knowledge gaps, are discussed in the present work. 

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 Coral reefs are increasingly experiencing stressful conditions, such as high temperatures, that cause corals to undergo bleaching, a process where they lose their photosynthetic algal symbionts. Bleaching threatens both corals’ survival and the health of the reef ecosystems they create. One possible mechanism for corals to resist bleaching is through association with stress-tolerant symbionts, which are resistant to bleaching but may be worse partners in mild conditions. Some corals have been found to associate with multiple symbiont species simultaneously, which potentially gives them access to the benefits of both stress-sensitive and -tolerant symbionts. However, within-host competition between symbionts may lead to competitive exclusion of one partner, and the consequences of associating with multiple partners simultaneously are not well understood. We modify a mechanistic model of coral-algal symbiosis to investigate the effect of environmental conditions on within-host competitive dynamics between stress-sensitive and -tolerant symbionts and the effect of access to a tolerant symbiont on the dynamics of recovery from bleaching. We found that the addition of a tolerant symbiont can increase host survival and recovery from bleaching in high-light conditions. Competitive exclusion of the tolerant symbiont occurred slowly at intermediate light levels. Interestingly, there were some cases of post-bleaching competitive exclusion after the tolerant symbiont had helped the host recover.