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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.

Coral reefs provide ecosystem benefits to millions of people but are threatened by rapid environmental change and ever-increasing human pressures. Restoration is becoming a priority strategy for coral reef conservation, yet implementation remains challenging and it is becoming increasingly apparent that indirect conservation and restoration approaches will not ensure the long-term sustainability of coral reefs. The important role of environmental conditions in restoration practice are currently undervalued, carrying substantial implications for restoration success. Giving paramount importance to environmental conditions, particularly during the pre-restoration planning phase, has the potential to bring about considerable improvements in coral reef restoration and innovation. This Essay argues that restoration risk may be reduced by adopting an environmentally aware perspective that gives historical, contemporary, and future context to restoration decisions. Such an approach will open up new restoration opportunities with improved sustainability that have the capacity to dynamically respond to environmental trajectories. Coral reef restoration faces many challenges. This Essay advocates for prioritizing environmental and climatic considerations to increase the sustainability of future coral reefs and open up opportunities for new restoration approaches. [ABSTRACT FROM AUTHOR]

This document is a correction notice for an article titled "The role and risks of selective adaptation in extreme coral habitats" published in Nature Communications. The correction addresses errors in the calculation of the density of reef corals, which affected the density values shown in Figure 3e and the statistical results reported in the legend for Figure 3 and in the Results section. The corrected version of Figure 3 and the corrected statistical values have been updated in both the HTML and PDF versions of the article. Supplementary information and updated source data are also provided. [Extracted from the article]

Simple Summary: When species from one place invade and settle in another, it can cause serious problems for the local environment. These invasions, known as bio-invasions, disrupt natural ecosystems and can lead to major changes. The Mediterranean Sea is especially at risk because the water conditions are changing rapidly due to climate change, which, coupled with the opening of the Suez Canal, creates an appropriate environment for species from the Red Sea to move in. In May 2023, divers found a type of soft coral called Dendronephthya, that is new to the Mediterranean Sea near Israel. This coral is normally found in the Indo-Pacific region and is common in the Red Sea. Using molecular and morphological analysis, we confirmed the identity of the coral. Because this coral can attach swiftly to surfaces and grow quickly, it is expected to spread rapidly and become more common throughout the Mediterranean Sea. Bio-invasions have the potential to provoke cascade effects that can disrupt natural ecosystems and cause ecological regime shifts. The Mediterranean Sea is particularly prone to bio-invasions as the changing water conditions, evoked by climate change, are creating advantageous conditions for Lessepsian migrants from the Red Sea. Recently, in May 2023, a new alien species was documented in the Mediterranean Sea—a soft coral of the genus Dendronephthya. This discovery was made by divers conducting 'Long-Term Ecological Research' surveys, along the coast of Israel, at a depth of 42 m. Genetic and morphological testing suggest that the species identity may be Dendronepthya hemprichi, an Indo-Pacific coral, common in the Red Sea. According to life history traits of this species, such as accelerated attachment to available surfaces and fast growth, we expect it to rapidly expand its distribution and abundance across the Mediterranean Sea. [ABSTRACT FROM AUTHOR]

Ocean acidification caused by shifts in ocean carbonate chemistry resulting from increased atmospheric CO2 concentrations is threatening many calcifying organisms, including corals. Here we assessed autotrophy vs heterotrophy shifts in the Mediterranean zooxanthellate scleractinian coral Balanophyllia europaea acclimatized to low pH/high pCO2 conditions at a CO2 vent off Panarea Island (Italy). Dinoflagellate endosymbiont densities were higher at lowest pH Sites where changes in the distribution of distinct haplotypes of a host-specific symbiont species, Philozoon balanophyllum, were observed. An increase in symbiont C/N ratios was observed at low pH, likely as a result of increased C fixation by higher symbiont cell densities. δ13C values of the symbionts and host tissue reached similar values at the lowest pH Site, suggesting an increased influence of autotrophy with increasing acidification. Host tissue δ15N values of 0‰ strongly suggest that diazotroph N2 fixation is occurring within the coral tissue/mucus at the low pH Sites, likely explaining the decrease in host tissue C/N ratios with acidification. Overall, our findings show an acclimatization of this coral-dinoflagellate mutualism through trophic adjustment and symbiont haplotype differences with increasing acidification, highlighting that some corals are capable of acclimatizing to ocean acidification predicted under end-of-century scenarios. Low seawater pH impacts trophic dynamics in corals, increasing symbiont density and autotrophic/heterotrophic ratios and varying dinoflagellate haplotypes under ocean acidification. [ABSTRACT FROM AUTHOR]

Stony corals (order: Scleractinia) differ in growth form and structure. While stony corals have gained the ability to form their aragonite skeleton once in their evolution, the suite of proteins involved in skeletogenesis is different for different coral species. This led to the conclusion that the organic portion of their skeleton can undergo rapid evolutionary changes by independently evolving new biomineralization-related proteins. Here, we used liquid chromatography-tandem mass spectrometry to sequence skeletogenic proteins extracted from the encrusting temperate coral Oculina patagonica. We compare it to the previously published skeletal proteome of the branching subtropical corals Stylophora pistillata as both are regarded as highly resilient to environmental changes. We further characterized the skeletal organic matrix (OM) composition of both taxa and tested their effects on the mineral formation using a series of overgrowth experiments on calcite seeds. We found that each species utilizes a different set of proteins containing different amino acid compositions and achieve a different morphology modification capacity on calcite overgrowth. Our results further support the hypothesis that the different coral taxa utilize a species-specific protein set comprised of independent gene co-option to construct their own unique organic matrix framework. While the protein set differs between species, the specific predicted roles of the whole set appear to underline similar functional roles. They include assisting in forming the extracellular matrix, nucleation of the mineral and cell signaling. Nevertheless, the different composition might be the reason for the varying organization of the mineral growth in the presence of a particular skeletal OM, ultimately forming their distinct morphologies. [ABSTRACT FROM AUTHOR]

The ecological distribution of coral species from shallow to mesophotic reefs is dependent on light, which varies drastically among local environments. Current definitions of mesophotic coral ecosystems primarily rely on a 30‐m recreational SCUBA boundary to define the upper limits of the community; however, this boundary does not consider local conditions and physiological adaptions of coral species. Using in situ benthic imagery and chlorophyll fluorescence measurements, we examined species distribution and community similarity, as well as photoacclimatization of two common depth‐generalist species (Montastraea cavernosa and Porites astreoides) across shallow to mesophotic reef zones at Little Cayman Island. Photoquadrat image analysis revealed a significant shift in coral species assemblages between 25 and 35 m, which was accompanied by a 30% drop in available surface light, suggesting light is a key driver of coral community composition. Patterns of photoacclimatization across depths differed significantly between the two coral species, with available surface light and the quantum yield of photochemistry in photosystem II found to be significant determinants of each species' abundance. These results provide valuable baseline data on coral community composition across a broad depth gradient in Little Cayman that can contribute to a growing body of evidence to set an upper boundary of mesophotic reefs based on light availability and photoacclimatization potential of depth‐generalist species. [ABSTRACT FROM AUTHOR]

Understanding the formation of the coral skeleton has been a common subject uniting various marine and materials study fields. Two main regions dominate coral skeleton growth: Rapid Accretion Deposits (RADs) and Thickening Deposits (TDs). These have been extensively characterized at the 2D level, but their 3D characteristics are still poorly described. Here, we present an innovative approach to combine synchrotron phase contrast-enhanced microCT (PCE-CT) with artificial intelligence (AI) to explore the 3D architecture of RADs and TDs within the coral skeleton. As a reference study system, we used recruits of the stony coral Stylophora pistillata from the Red Sea, grown under both natural and simulated ocean acidification conditions. We thus studied the recruit's skeleton under both regular and morphologically-altered acidic conditions. By imaging the corals with PCE-CT, we revealed the interwoven morphologies of RADs and TDs. Deep-learning neural networks were invoked to explore AI segmentation of these regions, to overcome limitations of common segmentation techniques. This analysis yielded highly-detailed 3D information about the RAD's and TD's architecture. Our results demonstrate how AI can be used as a powerful tool to obtain 3D data essential for studying coral biomineralization and for exploring the effects of environmental change on coral growth. [ABSTRACT FROM AUTHOR]

Background: Maternal mRNA provisioning of oocytes regulates early embryogenesis. Maternal transcripts are degraded as zygotic genome activation (ZGA) intensifies, a phenomenon known as the maternal-to-zygotic transition (MZT). Here, we examine gene expression over nine developmental stages in the Pacific rice coral, Montipora capitata, from eggs and embryos at 1, 4, 9, 14, 22, and 36 h-post-fertilization (hpf), as well as swimming larvae (9d), and adult colonies. Results: Weighted Gene Coexpression Network Analysis revealed four expression peaks, identifying the maternal complement, two waves of the MZT, and adult expression. Gene ontology enrichment revealed maternal mRNAs are dominated by cell division, methylation, biosynthesis, metabolism, and protein/RNA processing and transport functions. The first MZT wave occurs from ~4-14 hpf and is enriched in terms related to biosynthesis, methylation, cell division, and transcription. In contrast, functional enrichment in the second MZT wave, or ZGA, from 22 hpf-9dpf, includes ion/peptide transport and cell signaling. Finally, adult expression is enriched for functions related to signaling, metabolism, and ion/peptide transport. Our proposed MZT timing is further supported by expression of enzymes involved in zygotic transcriptional repression (Kaiso) and activation (Sox2), which peak at 14 hpf and 22 hpf, respectively. Further, DNA methylation writing (DNMT3a) and removing (TET1) enzymes peak and remain stable past ~4 hpf, suggesting that methylome programming occurs before 4 hpf. Conclusions: Our high-resolution insight into the coral maternal mRNA and MZT provides essential baseline information to understand parental carryover effects and the sensitivity of developmental success under increasing environmental stress. [ABSTRACT FROM AUTHOR]

The integrity of coral reefs worldwide is jeopardized by ocean acidification (OA). Most studies conducted so far have focused on the vulnerability to OA of corals inhabiting shallow reefs while nothing is currently known about the response of mesophotic scleractinian corals. In this study, we assessed the susceptibility to OA of corals, together with their algal partners, inhabiting a wide depth range. We exposed fragments of the depth generalist coral Stylophora pistillata collected from either 5 or 45 m to simulated future OA conditions, and assessed key molecular, physiological and photosynthetic processes influenced by the lowered pH. Our comparative analysis reveals that mesophotic and shallow S. pistillata corals are genetically distinct and possess different symbiont types. Under the exposure to acidification conditions, we observed a 50% drop of metabolic rate in shallow corals, whereas mesophotic corals were able to maintain unaltered metabolic rates. Overall, our gene expression and physiological analyses show that mesophotic corals possess a greater capacity to cope with the effects of OA compared to their shallow counterparts. Such capability stems from physiological characteristics (i.e., biomass and lipids energetics), a greater capacity to regulate cellular acid–base parameters, and a higher baseline expression of cell adhesion and extracellular matrix genes. Moreover, our gene expression analysis suggests that the enhanced symbiont photochemical efficiency under high pCO2 levels could prevent acidosis of the host cells and it could support a greater translocation of photosynthates, increasing the energy pool available to the host. With this work, we provide new insights on the response to OA of corals living at mesophotic depths. Our investigation discloses key genetic and physiological traits underlying the potential for corals to cope with future OA conditions. [ABSTRACT FROM AUTHOR]

With coral reefs declining globally, resilience of these ecosystems hinges on successful coral recruitment. However, knowledge of the acclimatory and/or adaptive potential in response to environmental challenges such as ocean acidification (OA) in earliest life stages is limited. Our combination of physiological measurements, microscopy, computed tomography techniques and gene expression analysis allowed us to thoroughly elucidate the mechanisms underlying the response of early-life stages of corals, together with their algal partners, to the projected decline in oceanic pH. We observed extensive physiological, morphological and transcriptional changes in surviving recruits, and the transition to a less-skeleton/more-tissue phenotype. We found that decreased pH conditions stimulate photosynthesis and endosymbiont growth, and gene expression potentially linked to photosynthates translocation. Our unique holistic study discloses the previously unseen intricate net of interacting mechanisms that regulate the performance of these organisms in response to OA. [ABSTRACT FROM AUTHOR]

While recent strides have been made in understanding the biological process by which stony corals calcify, much remains to be revealed, including the ubiquity across taxa of specific biomolecules involved. Several proteins associated with this process have been identified through proteomic profiling of the skeletal organic matrix (SOM) extracted from three scleractinian species. However, the evolutionary history of this putative "biomineralization toolkit," including the appearance of these proteins' throughout metazoan evolution, remains to be resolved. Here we used a phylogenetic approach to examine the evolution of the known scleractinians' SOM proteins across the Metazoa. Our analysis reveals an evolutionary process dominated by the co-option of genes that originated before the cnidarian diversification. Each one of the three species appears to express a unique set of the more ancient genes, representing the independent co-option of SOM proteins, as well as a substantial proportion of proteins that evolved independently. In addition, in some instances, the different species expressed multiple orthologous proteins sharing the same evolutionary history. Furthermore, the non-random clustering of multiple SOM proteins within scleractinian-specific branches suggests the conservation of protein function between distinct species for what we posit is part of the scleractinian "core biomineralization toolkit." This "core set" contains proteins that are likely fundamental to the scleractinian biomineralization mechanism. From this analysis, we infer that the scleractinians' ability to calcify was achieved primarily through multiple lineage-specific protein expansions, which resulted in a new functional role that was not present in the parent gene. [ABSTRACT FROM AUTHOR]

Spherulites are radial distributions of acicular crystals, common in biogenic, geologic, and synthetic systems, yet exactly how spherulitic crystals nucleate and grow is still poorly understood. To investigate these processes in more detail, we chose scleractinian corals as a model system, because they are well known to form their skeletons from aragonite (CaCO 3) spherulites, and because a comparative study of crystal structures across coral species has not been performed previously. We observed that all 12 diverse coral species analyzed here exhibit plumose spherulites in their skeletons, with well-defined centers of calcification (CoCs), and crystalline fibers radiating from them. In 7 of the 12 species, we observed a skeletal structural motif not observed previously: randomly oriented, equant crystals, which we termed "sprinkles". In Acropora pharaonis , these sprinkles are localized at the CoCs, while in 6 other species, sprinkles are either layered at the growth front (GF) of the spherulites, or randomly distributed. At the nano- and micro-scale, coral skeletons fill space as much as single crystals of aragonite. Based on these observations, we tentatively propose a spherulite formation mechanism in which growth front nucleation (GFN) of randomly oriented sprinkles, competition for space, and coarsening produce spherulites, rather than the previously assumed slightly misoriented nucleations termed "non-crystallographic branching". Phase-field simulations support this mechanism, and, using a minimal set of thermodynamic parameters, are able to reproduce all of the microstructural variation observed experimentally in all of the investigated coral skeletons. Beyond coral skeletons, other spherulitic systems, from aspirin to semicrystalline polymers and chocolate, may also form according to the mechanism for spherulite formation proposed here. Understanding the fundamental mechanisms of spherulite nucleation and growth has broad ranging applications in the fields of metallurgy, polymers, food science, and pharmaceutical production. Using the skeletons of reef-building corals as a model system for investigating these processes, we propose a new spherulite growth mechanism that can not only explain the micro-structural diversity observed in distantly related coral species, but may point to a universal growth mechanism in a wide range of biologically and technologically relevant spherulitic materials systems. Image, graphical abstract [ABSTRACT FROM AUTHOR]

Reef-building corals, the major producers of biogenic calcium carbonate, form skeletons in a plethora of morphological forms. Here we studied skeletal modifications of Stylophora pistillata (clade 4) colonies that adapt to increasing depths with decreasing ambient light. The coral show characteristic transitions from spherical morphologies (shallow depths, 5 m deep) to flat and branching geometries (mesophotic depths, 60 m deep). Such changes are typically ascribed to the algal photosymbiont physiological feedback with the coral that host them. We find specific fine-scale skeletal variability in accretion of structure at shallow- and mesophotic depth morphotypes that suggest underlying genomic regulation of biomineralization pathways of the coral host. To explain this, we conducted comparative morphology-based analyses, including optical and electron microscopy, tomography and X-ray diffraction analysis coupled with a comprehensive transcriptomic analysis of S. pistillata. The samples originated from Gulf of Eilat in the Red Sea collected along a depth gradient from shallow to mesophotic depths (5 to 60 m). Additional samples were experimentally transplanted from 5 m to 60 m and from 60 m to 5 m. Interestingly, both morphologically and functionally, transplanted corals partly adapt by exhibiting typical depth-specific properties. In mesophotic depths, we find that the organic matrix fraction is enriched in the coralla, well matching the overrepresentation of transcripts encoding biomineralization "tool-kit" structural extracellularproteins that was observed. These results provide insights into the molecular mechanisms of calcification and skeletal adaptation that repeatedly allowed this coral group to adapt to a range of environments presumably with a rich geological past. Understanding the reef coral physiological plasticity under a rapidly changing climate is of crucial importance for the protection of coral reef ecosystems. Most of the reef corals operate near their upper limit of heat tolerance. A possible rescue for some coral species is migration to deeper, cooler mesophotic depths. However, gradually changing environmental parameters (especially light) along the depth gradient pose new adaptative stress on corals with largely unknown influences on the various biological molecular pathways. This work provides a first comprehensive analysis of changes in gene expression, including biomineralization "tool kit" genes, and reports the fine-scale microstructural and crystallographic skeletal details in S. pistillata collected in the Red Sea along a depth gradient spannign 5 to 60 m. Image, graphical abstract [ABSTRACT FROM AUTHOR]

Reef-building corals and their aragonite (CaCO3) skeletons support entire reef ecosystems, yet their formation mechanism is poorly understood. Here we used synchrotron spectromicroscopy to observe the nanoscale mineralogy of fresh, forming skeletons from six species spanning all reef-forming coral morphologies: Branching, encrusting, massive, and table. In all species, hydrated and anhydrous amorphous calcium carbonate nanoparticles were precursors for skeletal growth, as previously observed in a single species. The amorphous precursors here were observed in tissue, between tissue and skeleton, and at growth fronts of the skeleton, within a low-density nano- or microporous layer varying in thickness from 7 to 20 µm. Brunauer-Emmett-Teller measurements, however, indicated that the mature skeletons at the microscale were space-filling, comparable to single crystals of geologic aragonite. Nanoparticles alone can never fill space completely, thus ion-by-ion filling must be invoked to fill interstitial pores. Such ionby- ion diffusion and attachment may occur from the supersaturated calcifying fluid known to exist in corals, or from a dense liquid precursor, observed in synthetic systems but never in biogenic ones. Concomitant particle attachment and ion-by-ion filling was previously observed in synthetic calcite rhombohedra, but never in aragonite pseudohexagonal prisms, synthetic or biogenic, as observed here. Models for biomineral growth, isotope incorporation, and coral skeletons' resilience to ocean warming and acidification must take into account the dual formation mechanism, including particle attachment and ion-by-ion space filling. [ABSTRACT FROM AUTHOR]

Background: Coral reefs are among the most diverse, complex and densely populated marine ecosystems. To survive, morphologically simple and sessile cnidarians have developed mechanisms to catch prey, deter predators and compete with adjacent corals for space, yet the mechanisms underlying these functions are largely unknown. Here, we characterize the histology, toxic activity and gene expression patterns in two different types of tentacles from the scleractinian coral Galaxea fascilcularis – catch tentacles (CTs), used to catch prey and deter predators, and sweeper tentacles (STs), specialized tentacles used for territorial aggression. Results: STs exhibit more mucocytes and higher expression of mucin genes than CTs, and lack the ectodermal cilia used to deliver food to the mouth and remove debris. STs and CTs also express different sensory rhodopsin-like g-protein coupled receptors, suggesting they may employ different sensory pathways. Each tentacle type has a different complement of stinging cells (nematocytes), and the expression in the two tentacles of genes encoding structural nematocyte proteins suggests the stinging cells develop within the tentacles. CTs have higher neurotoxicity to blowfly larvae and hemolytic activity compared to the STs, consistent with a role in prey capture. In contrast, STs have higher phospholipase A2 activity, which we speculate may have a role in inducing tissue damage during territorial aggression. The expression of genes encoding cytolytic toxins (actinoporins) and phospholipases also differs between the tentacle types. Conclusions: These results show that the same organism utilizes two distinct tentacle types, each equipped with a different venom apparatus and toxin composition, for prey capture and defense and for territorial aggression. [ABSTRACT FROM AUTHOR]

Background. Reproductive biology and the evolutionary constraints acting on dispersal stages are poorly understood in many stony coral species. A key piece of missing information is egg and sperm gene expression. This is critical for broadcast spawning corals, such as our model, the Hawaiian species Montipora capitata, because eggs and sperm are exposed to environmental stressors during dispersal. Furthermore, parental effects such as transcriptome investment may provide a means for cross- or transgenerational plasticity and be apparent in egg and sperm transcriptome data. Methods. Here, we analyzed M. capitata egg and sperm transcriptomic data to address three questions: (1) Which pathways and functions are actively transcribed in these gametes? (2) How does sperm and egg gene expression differ from adult tissues? (3) Does gene expression differ between these gametes? Results. We show that egg and sperm display surprisingly similar levels of gene expression and overlapping functional enrichment patterns. These results may reflect similar environmental constraints faced by these motile gametes. We find significant differences in differential expression of egg vs. adult and sperm vs. adult RNA-seq data, in contrast to very few examples of differential expression when comparing egg vs. sperm transcriptomes. Lastly, using gene ontology and KEGG orthology data we show that both egg and sperm have markedly repressed transcription and translation machinery compared to the adult, suggesting a dependence on parental transcripts. We speculate that cell motility and calcium ion binding genes may be involved in gamete to gamete recognition in the water column and thus, fertilization. [ABSTRACT FROM AUTHOR]

Hard, or stony, corals make rocks that can, on geological time scales, lead to the formation of massive reefs in shallow tropical and subtropical seas. In both historical and contemporary oceans, reef‐building corals retain information about the marine environment in their skeletons, which is an organic–inorganic composite material. The elemental and isotopic composition of their skeletons is frequently used to reconstruct the environmental history of Earth's oceans over time, including temperature, pH, and salinity. Interpretation of this information requires knowledge of how the organisms formed their skeletons. The basic mechanism of formation of calcium carbonate skeleton in stony corals has been studied for decades. While some researchers consider coral skeletons as mainly passive recorders of ocean conditions, it has become increasingly clear that biological processes play key roles in the biomineralization mechanism. Understanding the role of the animal in living stony coral biomineralization and how it evolved has profound implications for interpreting environmental signatures in fossil corals to understand past ocean conditions. Here we review historical hypotheses and discuss the present understanding of how corals evolved and how their skeletons changed over geological time. We specifically explain how biological processes, particularly those occurring at the subcellular level, critically control the formation of calcium carbonate structures. We examine the different models that address the current debate including the tissue–skeleton interface, skeletal organic matrix, and biomineralization pathways. Finally, we consider how understanding the biological control of coral biomineralization is critical to informing future models of coral vulnerability to inevitable global change, particularly increasing ocean acidification. [ABSTRACT FROM AUTHOR]

In reef-building corals, larval settlement and its rapid calcification provides a unique opportunity to study the bio-calcium carbonate formation mechanism involving skeleton morphological changes. Here we investigate the mineral formation of primary polyps, just after settlement, in two species of the pocilloporoid corals: Stylophora pistillata (Esper, 1797) and Pocillopora acuta (Lamarck, 1816). We show that the initial mineral phase is nascent Mg-Calcite, with rod-like morphology in P. acuta , and dumbbell morphology in S. pistillata. These structures constitute the first layer of the basal plate which is comparable to Rapid Accretion Deposits (Centers of Calcification, CoC) in adult coral skeleton. We found also that the rod-like/dumbbell Mg-Calcite structures in subsequent growth step will merge into larger aggregates by deposition of aragonite needles. Our results suggest that a biologically controlled mineralization of initial skeletal deposits occurs in three steps: first, vesicles filled with divalent ions are formed intracellularly. These vesicles are then transferred to the calcification site, forming nascent Mg-Calcite rod/pristine dumbbell structures. During the third step, aragonite crystals develop between these structures forming spherulite-like aggregates. Coral settlement and recruitment periods are highly sensitive to environmental conditions. Successful mineralization during these periods is vital and influences the coral's chances of survival. Therefore, understanding the exact mechanism underlying carbonate precipitation is highly important. Here, we used in vivo microscopy, spectroscopy and molecular methods to provide new insights into mineral development. We show that the primary polyp's mineral arsenal consists of two types of minerals: Mg-Calcite and aragonite. In addition, we provide new insights into the ion pathway by showing that divalent ions are concentrated in intracellular vesicles and are eventually deposited at the calcification site. [ABSTRACT FROM AUTHOR]

Abstract: Stony corals construct their aragonite skeleton by calcium carbonate precipitation, in a process recently suggested to be biologically controlled. Amorphous calcium carbonate and small amounts of calcite are also reported recently, however, their functional role is unknown. Coral acid‐rich proteins (CARPs) are extracted from the coral skeleton and are shown to be active in calcium carbonate precipitation in vitro. However, individual function of these proteins in coral mineralization is not known. Here, the regulatory activity of the aspartate‐rich CARP3 protein is examined. The whole protein and two peptides representing its acidic domain and its variable domain are used in CaCO3 precipitation reactions from Mg‐rich solutions. The biomolecules alter crystallization pathways, promoting Mg‐calcite in place of aragonite, with the acidic peptide capable of eradicating aragonite formation. The activity of CARP3 and its representative peptides is exerted from disordered CaCO3 mineral phases, coating the crystals formed, as shown by 2D 1H–13C heteronuclear correlation nuclear magnetic resonance (NMR) measurements, localizing organic protons in atomic proximity to disordered carbonate carbons. The structures of the protein and individual domains as derived from NMR measurements and folding calculations and their amino acid compositions are discussed in the context of their observed activity and its implication to mineralization in hard corals. [ABSTRACT FROM AUTHOR]

Do corals form their skeletons by precipitation from solution or by attachment of amorphous precursor particles as observed in other minerals and biominerals? The classical model assumes precipitation in contrast with observed "vital effects," that is, deviations from elemental and isotopic compositions at thermodynamic equilibrium. Here, we show direct spectromicroscopy evidence in Stylophora pistillata corals that two amorphous precursors exist, one hydrated and one anhydrous amorphous calcium carbonate (ACC); that these are formed in the tissue as 400-nm particles; and that they attach to the surface of coral skeletons, remain amorphous for hours, and finally, crystallize into aragonite (CaCO3). We show in both coral and synthetic aragonite spherulites that crystal growth by attachment of ACC particles is more than 100 times faster than ion-by-ion growth from solution. Fast growth provides a distinct physiological advantage to corals in the rigors of the reef, a crowded and fiercely competitive ecosystem. Corals are affected by warming-induced bleaching and postmortem dissolution, but the finding here that ACC particles are formed inside tissue may make coral skeleton formation less susceptible to ocean acidification than previously assumed. If this is how other corals form their skeletons, perhaps this is how a few corals survived past CO2 increases, such as the Paleocene-Eocene Thermal Maximum that occurred 56 Mya. [ABSTRACT FROM AUTHOR]

We experimentally examined the in situ, long-term effects of flow on the coral Pocillopora verrucosa over a 2-yr period. Eighteen coral nubbins were positioned on stages protected from the ambient flow with transparent walls. Six of the corals were exposed to "enhanced flow" with underwater pumps (15-20 cm s-1), while another other six were grown under "reduced-flow" conditions (~ 1 cm s-1), and a further six nubbins were set up as a control treatment exposed to ambient natural flow conditions on stages without walls. Mortality was 50% in the reduced-flow experiment. Compared with the reduced-flow and the control treatments, colonies growing in enhanced-flow conditions developed a more compact morphology and had significantly higher chlorophyll and protein concentrations, a higher density of zooxanthellae, and, most importantly, higher reproductive output. However, corals grown in reduced-flow conditions had lower skeleton density compared with those grown under ambient flow or enhanced flow. Flow rate had no measurable influence on average pH at the site of calcification as monitored by skeletal boron isotopic composition (δ11B). Hence, the skeletal δ11B-pH proxy in this coral appears to be independent of flow and the biological attributes that are modulated by flow, such as zooxanthellae density, chlorophyll concentrations, and rates of photosynthesis, respiration, and calcification. Calcification site pH in all colonies was raised by ±0.3 relative to ambient seawater pH. Together with light, flow should be considered a key abiotic factor determining core biological characteristics of P. verrucosa. [ABSTRACT FROM AUTHOR]

[Display omitted] • Porites astreoides corals show light-driven micro-skeletal differences across depths. • Tomographic reconstructions reveal an analogous internal mineral distribution. • Transcriptional changes show different regulation of metabolism and stress response. • Genetic and symbiont homogeneity suggest connectivity across a broad depth range. • These findings shed light on mesophotic reefs as climate refugia. The widespread decline of shallow-water coral reefs has fueled interest in assessing whether mesophotic reefs can act as refugia replenishing deteriorated shallower reefs through larval exchange. Here we explore the morphological and molecular basis facilitating survival of planulae and adults of the coral Porites astreoides (Lamarck, 1816; Hexacorallia: Poritidae) along the vertical depth gradient in Bermuda. We found differences in micro-skeletal features such as bigger calyxes and coarser surface of the skeletal spines in shallow corals. Yet, tomographic reconstructions reveal an analogous mineral distribution between shallow and mesophotic adults, pointing to similar skeleton growth dynamics. Our study reveals patterns of host genetic connectivity and minimal symbiont depth-zonation across a broader depth range than previously known for this species in Bermuda. Transcriptional variations across life stages showed different regulation of metabolism and stress response functions, unraveling molecular responses to environmental conditions at different depths. Overall, these findings increase our understanding of coral acclimatory capability across broad vertical gradients, ultimately allowing better evaluation of the refugia potential of mesophotic reefs. [ABSTRACT FROM AUTHOR]

Stony corals are colonial cnidarians that sustain the most biodiverse marine ecosystems on Earth: coral reefs. Despite their ecological importance, little is known about the cell types and molecular pathways that underpin the biology of reef-building corals. Using single-cell RNA sequencing, we define over 40 cell types across the life cycle of Stylophora pistillata. We discover specialized immune cells, and we uncover the developmental gene expression dynamics of calcium-carbonate skeleton formation. By simultaneously measuring the transcriptomes of coral cells and the algae within them, we characterize the metabolic programs involved in symbiosis in both partners. We also trace the evolution of these coral cell specializations by phylogenetic integration of multiple cnidarian cell type atlases. Overall, this study reveals the molecular and cellular basis of stony coral biology. [Display omitted] • Whole-organism single-cell analysis of the stony coral Stylophora pistillata • Skeleton formation and symbiosis-associated gene expression dynamics • Identification of immune cell programs in Stylophora pistillata • Conserved broad cell type identities across cnidarian lineages Over 40 cell types across the life cycle of Stylophora pistillata , a stony coral, are identified through the use of single-cell RNA sequencing. From this reference atlas, the molecular pathways underpinning coral reef building, specialized immune cells, and the metabolic programs involved in symbiosis between coral and algae partners are described. [ABSTRACT FROM AUTHOR]

• CARP3 induces surface roughness on CaCO 3 crystals formed from solution. • CARP3 polymorph selection activity is highly influenced by presence of Mg2+ ions. • CARP3 inhibits calcite and favors vaterite formation in calcite growth conditions. • Vaterite polymorph selection is CARP3 concentration dependent in Mg2+ ions absence. • CARP3 favors CaCO 3 crystallization over stabilization of ACC or ACC-H 2 O. Corals and other biomineralizing organisms use proteins and other molecules to form different crystalline polymorphs and biomineral structures. In corals, it's been suggested that proteins such as Coral Acid Rich Proteins (CARPs) play a major role in the polymorph selection of their calcium carbonate (CaCO 3) aragonite exoskeleton. To date, four CARPs (1–4) have been characterized: each with a different amino acid composition and different temporal and spatial expression patterns during coral developmental stages. Interestingly, CARP3 is able to alter crystallization pathways in vitro , yet its function in this process remains enigmatic. To better understand the CARP3 function, we performed two independent in vitro CaCO 3 polymorph selection experiments using purified recombinant CARP3 at different concentrations and at low or zero Mg2+ concentration. Our results show that, in the absence of Mg2+, CARP3 selects for the vaterite polymorph and inhibits calcite. However, in the presence of a low concentration of Mg2+ and CARP3 both Mg-calcite and vaterite are formed, with the relative amount of Mg-calcite increasing with CARP3 concentration. In all conditions, CARP3 did not select for the aragonite polymorph, which is the polymorph associated to CARP3 in vivo , even in the presence of Mg2+ (Mg:Ca molar ratio equal to 1). These results further emphasize the importance of Mg:Ca molar ratios similar to that in seawater (Mg:Ca equal to 5) and the activity of the biological system in a aragonite polymorph selection in coral skeleton formation. [ABSTRACT FROM AUTHOR]