Transcriptional profiles inferring thermal stress responses of the coral Oculina patagonica from the Eastern Mediterranean Sea

During the past several decades, corals worldwide have been dealing with a considerable increase in water temperature due to climate change, which is predicted to increase the frequency of coral bleaching and mass mortality events. Nevertheless, corals show differences in stress susceptibility and they are not all affected evenly. The symbiotic coral Oculina patagonica from the Eastern Mediterranean Sea can thrive in relatively unstable environments and is considered a stress-tolerant species. In this study, baseline expression and temporal dynamics of induction of a 70-kDa heat shock protein (HSP70) after an acute heat stress were analyzed in O. patagonica to investigate the influence of its peculiar physiological traits on stress responsiveness. Furthermore, data collected were further discussed within a comparative analysis with similar findings reported in 5 temperate corals of the Mediterranean Sea (Franzellitti et al., 2018). Results show that O. patagonica hsp70 transcriptional response aligns with the formerly observed high resistance for elevated sea water temperatures of this species. The multispecies comparison shows that hsp70 expression varies in accordance with the stress sensitivity of coral populations inhabiting different thermal environments and possessing different trophic strategies and morphologies. This study also reports an analysis of the post heat-stress transcriptional regulation of transcripts related to energy metabolism (gadph), redox regulation (sod), and DNA damage (bcl-2 and bax), disclosing the time line of the events occurring in O. patagonica in response to an acute heat stress, which aligns with its quick recovery from bleaching. These molecular processes analysis is particularly demanding for corals inhabiting the Mediterranean Sea, in light of projected scenarios of anthropogenic global change

Artificial Intelligence as a Tool to Study the 3D Skeletal Architecture in Newly Settled Coral Recruits: Insights into the Effects of Ocean Acidification on Coral Biomineralization

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

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

Seawater carbonate chemistry and proportion of transcriptome changing, coral protein concentration, respiration rates, algal photosynthetic parameters

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 meters 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

Seawater carbonate chemistry and 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

The role and risks of selective adaptation in extreme coral habitats

Abstract 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

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

Summary: 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

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

Summary: 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