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Abstract Epigenetic modifications directly regulate the patterns of gene expression by altering DNA accessibility and chromatin structure. A knowledge gap is presented by the need to directly measure these modifications, especially for unannotated organisms with unknown primary histone sequences. In the present work, we developed and applied a novel workflow for identifying and annotating histone proteoforms directly from mass spectrometry-based measurements for the endangered Caribbean coral Acropora cervicornis. Combining high-accuracy de novo top-down and bottom-up analysis based on tandem liquid chromatography, trapped ion mobility spectrometry, non-ergodic electron-based fragmentation, and high-resolution mass spectrometry, near complete primary sequence (up to 99%) and over 86 post-translational modification annotations were obtained from pull-down histone fractions. In the absence of reliable genome annotations, H2A, H2B, and H4 histone sequences and the annotation of the post-translational modifications of the stressed A. cervicornis coral allow for a better understanding of chromatin remodeling and new strategies for targeting intervention and restoration of endangered reef corals. 

Abstract Histone post-translational modifications (PTMs) participate in the dynamic regulation of chromatin structure and function, through their chemical nature and specific location within the histone sequence. Alternative analytical approaches for histone PTM studies are required to facilitate the differentiation between ubiquitously present isomers and the detection of low-abundance PTMs Here, we report a high-sensitivity bottom-up method based on nano-liquid chromatography (nLC), trapped ion mobility spectrometry (TIMS), data-dependent acquisition (DDA), parallel accumulation-serial fragmentation (PASEF), and high-resolution time-of-flight tandem mass spectrometry (ToF-MS/MS) for the analysis of histone PTMs. This method was tested in a threatened coral species, the staghorn coral Acropora cervicornis, during an episode of acute thermal stress. The obtained results allowed for the identification of PTM changes in core histones involved in the coral’s heat response. Compared to traditional LC-MS/MS approaches, the incorporation of TIMS and ddaPASEF MS/MS resulted in a highly specific and sensitive method with a wide dynamic range (6 orders of magnitude). This depth of analysis allows for the simultaneous measurement of low-abundance PTM signatures relative to the unmodified form. An added advantage is the ability to mass- and mobility-isolate prior to peptide sequencing, resulting in higher confidence identification of epigenetic markers associated with heat stress in corals (e.g. increased H4 4–17 with 2ac and 3ac, and decreases in H4 4–17 K12ac, K16ac, H4 K20me2, and H2A K5ac, K7ac, K9ac, K12ac, K14ac, and K74ac). 

Abstract The plastic ability for a range of phenotypes to be exhibited by the same genotype allows organisms to respond to environmental variation and may modulate fitness in novel environments. Differing capacities for phenotypic plasticity within a population, apparent as genotype by environment interactions (GxE), can therefore have both ecological and evolutionary implications. Epigenetic gene regulation alters gene function in response to environmental cues without changes to the underlying genetic sequence and likely mediates phenotypic variation. DNA methylation is currently the most well described epigenetic mechanism and is related to transcriptional homeostasis in invertebrates. However, evidence quantitatively linking variation in DNA methylation with that of phenotype is lacking in some taxa, including reef‐building corals. In this study, spatial and seasonal environmental variation in Bonaire, Caribbean Netherlands was utilized to assess relationships between physiology and DNA methylation profiles within genetic clones across different genotypes ofAcropora cervicornisandA. palmatacorals. The physiology of both species was highly influenced by environmental variation compared to the effect of genotype. GxE effects on phenotype were only apparent inA. cervicornis. DNA methylation in both species differed between genotypes and seasons and epigenetic variation was significantly related to coral physiological metrics. Furthermore, plastic shifts in physiology across seasons were significantly positively correlated with shifts in DNA methylation profiles in both species. These results highlight the dynamic influence of environmental conditions and genetic constraints on the physiology of two important Caribbean coral species. Additionally, this study provides quantitative support for the role of epigenetic DNA methylation in mediating phenotypic plasticity in invertebrates. 

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. 

Abstract The global impacts of climate change are evident in every marine ecosystem. On coral reefs, mass coral bleaching and mortality have emerged as ubiquitous responses to ocean warming, yet one of the greatest challenges of this epiphenomenon is linking information across scientific disciplines and spatial and temporal scales. Here we review some of the seminal and recent coral‐bleaching discoveries from an ecological, physiological, and molecular perspective. We also evaluate which data and processes can improve predictive models and provide a conceptual framework that integrates measurements across biological scales. Taking an integrative approach across biological and spatial scales, using for example hierarchical models to estimate major coral‐reef processes, will not only rapidly advance coral‐reef science but will also provide necessary information to guide decision‐making and conservation efforts. To conserve reefs, we encourage implementing mesoscale sanctuaries (thousands of km²) that transcend national boundaries. Such networks of protected reefs will provide reef connectivity, through larval dispersal that transverse thermal environments, and genotypic repositories that may become essential units of selection for environmentally diverse locations. Together, multinational networks may be the best chance corals have to persist through climate change, while humanity struggles to reduce emissions of greenhouse gases to net zero. 

Phenotypic plasticity is defined as a property of individual genotypes to produce different phenotypes when exposed to different environmental conditions. This ability may be expressed at behavioral, biochemical, physiological, and/or developmental levels, exerting direct influence over species' demographic performance. In reef-building corals, a group critically threatened by global change in the Anthropocene, non-genetic mechanisms (i.e., epigenetic and microbiome variation) have been shown to participate in plastic physiological responses to environmental change. Yet, the precise way in which these mechanisms interact, contribute to such responses, and their adaptive potential is still obscure. The present work aims to fill this gap by using a multi-omics approach to elucidate the contribution and interconnection of the mechanisms modulating phenotypic plasticity in staghorn coral (Acropora cervicornis) clones subject to different depth conditions. Results show changes in lipidome, epigenome and transcriptome, but not in symbiotic and microbial communities. In addition, a potential shift toward a more heterotrophic feeding behavior was evidenced in corals at the deeper site. These observations are consistent with a multi-mechanism modulation of rapid acclimation in corals, underscoring the complexity of this process and the importance of a multifactorial approach to inform potential intervention to enhance coral adaptive capacity.