Genomic, morphological, and physiological insights into coral acclimation along the depth gradient following an in situ reciprocal transplantation of planulae.

Mesophotic coral reefs have been proposed as refugia for corals, providing shelter and larval propagules for shallow water reefs that are disproportionately challenged by global climate change and local anthropogenic stressors. For mesophotic reefs to be a viable refuge, firstly, deep origin larvae must survive on shallow reefs and, secondly, the two environments must be physically connected. This study tested the first condition. Planulae of the reef-building coral Stylophora pistillata from 5-8 and 40-44 m depth in the Gulf of Aqaba were tested in a long-term reciprocal transplantation experiment for their ability to settle and acclimate to depth in situ. We assessed survival rates, photochemical, physiological, and morphological characteristics in juveniles grown at either their parental origin or transplantation depth. Differences in gene expression patterns were compared between mesophotic and shallow corals at the adult, juvenile, and planula life stages. We found high mortality rates among all mesophotic-origin planulae, irrespective of translocation depth. Gene expression patterns suggested that deep planulae lacked settlement competency and experienced increased developmental stress upon release. For surviving shallow origin juveniles, symbiont photochemical acclimation to depth occurred within 8 days, with symbiont communities showing changes in photochemical traits without algal symbiont shuffling. However, coral host physiological and morphological acclimation towards the typical deep phenotype was incomplete within 60 days. Gene expression was influenced by both life stage and depth. A set of differentially expressed genes (DEGs) associated with initial stress responses following transplantation, latent stress response, and environmental effects of depth was identified. This study therefore refutes the Deep Reef Refugia Hypothesis, as the potential for mesophotic-origin S. pistillata planulae to recruit to the shallow reef is low. The potential remains for shallow planulae to survive at mesophotic depths.

A novel in vivo system to study coral biomineralization in the starlet sea anemone, Nematostella vectensis.

Coral conservation requires a mechanistic understanding of how environmental stresses disrupt biomineralization, but progress has been slow, primarily because corals are not easily amenable to laboratory research. Here, we highlight how the starlet sea anemone, Nematostella vectensis, can serve as a model to interrogate the cellular mechanisms of coral biomineralization. We have developed transgenic constructs using biomineralizing genes that can be injected into Nematostella zygotes and designed such that translated proteins may be purified for physicochemical characterization. Using fluorescent tags, we confirm the ectopic expression of the coral biomineralizing protein, SpCARP1, in Nematostella. We demonstrate via calcein staining that SpCARP1 concentrates calcium ions in Nematostella, likely initiating the formation of mineral precursors, consistent with its suspected role in corals. These results lay a fundamental groundwork for establishing Nematostella as an in vivo system to explore the evolutionary and cellular mechanisms of coral biomineralization, improve coral conservation efforts, and even develop novel biomaterials.

Morphological and genetic mechanisms underlying the plasticity of the coral Porites astreoides across depths in Bermuda.

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.

Physiological and morphological plasticity in Stylophora pistillata larvae from Eilat, Israel, to shallow and mesophotic light conditions.

Mesophotic reefs have been proposed as climate change refugia but are not synonymous ecosystems with shallow reefs and remain exposed to anthropogenic impacts. Planulae from the reef-building coral Stylophora pistillata, Gulf of Aqaba, from 5- and 45-m depth were tested ex situ for capacity to settle, grow, and acclimate to reciprocal light conditions. Skeletons were scanned by phase contrast-enhanced micro-CT to study morphology. Deep planulae had reduced volume, smaller diameter on settlement, and greater algal symbiont density. Light conditions did not have significant impact on settlement or mortality rates. Photosynthetic acclimation of algal symbionts was evident within 21-35 days after settlement but growth rate and polyp development were slower for individuals translocated away from their parental origin compared to controls. Though our data reveal rapid symbiont acclimation, reduced growth rates and limited capacity for skeletal modification likely limit the potential for mesophotic larvae to settle on shallow reefs.

The role and risks of selective adaptation in extreme coral habitats.

The alarming rate of climate change demands new management strategies to protect coral reefs. Environments such as mangrove lagoons, characterized by extreme variations in multiple abiotic factors, are viewed as potential sources of stress-tolerant corals for strategies such as assisted evolution and coral propagation. However, biological trade-offs for adaptation to such extremes are poorly known. Here, we investigate the reef-building coral Porites lutea thriving in both mangrove and reef sites and show that stress-tolerance comes with compromises in genetic and energetic mechanisms and skeletal characteristics. We observe reduced genetic diversity and gene expression variability in mangrove corals, a disadvantage under future harsher selective pressure. We find reduced density, thickness and higher porosity in coral skeletons from mangroves, symptoms of metabolic energy redirection to stress response functions. These findings demonstrate the need for caution when utilizing stress-tolerant corals in human interventions, as current survival in extremes may compromise future competitive fitness.

Genetic and physiological traits conferring tolerance to ocean acidification in mesophotic corals.

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.

Combined responses of primary coral polyps and their algal endosymbionts to decreasing seawater pH.

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.

Physiological characteristics of Stylophora pistillata larvae across a depth gradient.

Depth related parameters, specifically light, affect different aspects of corals physiology, including fluorescence. GFP-like pigments found in many coral species have been suggested to serve a variety of functions, including photo-protection and photo-enhancement. Using fluorescence imaging and molecular analysis, we further investigated the role of these proteins on the physiology of the coral Stylophora pistillata and its algal partners. Fluorescence was found to differ significantly between depths for larvae and adult colonies. Larvae from the shallow reef presented a higher GFP expression and a greater fluorescence intensity compared to the larvae from the mesophotic reef, reflecting the elevated need for photo-protection against high light levels characteristic of the shallow reef, thus supporting the "sunscreen" hypothesis. Additionally, given the lower but still occurring protein expression under non-damaging low light conditions, our results suggest that GFP-like proteins might act to regulate the amount of photosynthetically usable light for the benefit of the symbiotic algae. Moreover, we propose that the differences in GFP expression and green fluorescence between shallow and deep larvae indicate that the GFPs within coral larvae might serve to attract and retain different symbiont clades, increasing the chances of survival when encountering new environments.

Energy Sources of the Depth-Generalist Mixotrophic Coral Stylophora pistillata.

Energy sources of corals, ultimately sunlight and plankton availability, change dramatically from shallow to mesophotic (30-150 m) reefs. Depth-generalist corals, those that occupy both of these two distinct ecosystems, are adapted to cope with such extremely diverse conditions. In this study, we investigated the trophic strategy of the depth-generalist hermatypic coral Stylophora pistillata and the ability of mesophotic colonies to adapt to shallow reefs. We compared symbiont genera composition, photosynthetic traits and the holobiont trophic position and carbon sources, calculated from amino acids compound-specific stable isotope analysis (AA-CSIA), of shallow, mesophotic and translocated corals. This species harbors different Symbiodiniaceae genera at the two depths: Cladocopium goreaui (dominant in mesophotic colonies) and Symbiodinium microadriaticum (dominant in shallow colonies) with a limited change after transplantation. This allowed us to determine which traits stem from hosting different symbiont species compositions across the depth gradient. Calculation of holobiont trophic position based on amino acid δ15N revealed that heterotrophy represents the same portion of the total energy budget in both depths, in contrast to the dogma that predation is higher in corals growing in low light conditions. Photosynthesis is the major carbon source to corals growing at both depths, but the photosynthetic rate is higher in the shallow reef corals, implicating both higher energy consumption and higher predation rate in the shallow habitat. In the corals transplanted from deep to shallow reef, we observed extensive photo-acclimation by the Symbiodiniaceae cells, including substantial cellular morphological modifications, increased cellular chlorophyll a, lower antennae to photosystems ratios and carbon signature similar to the local shallow colonies. In contrast, non-photochemical quenching remains low and does not increase to cope with the high light regime of the shallow reef. Furthermore, host acclimation is much slower in these deep-to-shallow transplanted corals as evident from the lower trophic position and tissue density compared to the shallow-water corals, even after long-term transplantation (18 months). Our results suggest that while mesophotic reefs could serve as a potential refuge for shallow corals, the transition is complex, as even after a year and a half the acclimation is only partial.