Description: 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.

Description: 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.

Description: 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.

Description: Corals exert a strong biological control over their calcification processes, but there is a lack of knowledge on their capability of long-term acclimatization to ocean acidification (OA). We used a dual geochemical proxy approach to estimate the calcifying fluid pH (pHcf) and carbonate chemistry of a Mediterranean coral (Balanophyllia europaea) naturally growing along a pH gradient (range: pHTS 8.07–7.74). The pHcf derived from skeletal boron isotopic composition (δ11B) was 0.3–0.6 units above seawater values and homogeneous along the gradient (mean ± SEM: Site 1 = 8.39 ± 0.03, Site 2 = 8.34 ± 0.03, Site 3 = 8.34 ± 0.02). Also carbonate ion concentration derived from B/Ca was homogeneous [mean ± SEM (μmol kg–1): Site 1 = 579 ± 34, Site 2 = 541 ± 27, Site 3 = 568 ± 30] regardless of seawater pH. Furthermore, gross calcification rate (GCR, mass of CaCO3 deposited on the skeletal unit area per unit of time), estimated by a “bio-inorganic model” (IpHRAC), was homogeneous with decreasing pH. The homogeneous GCR, internal pH and carbonate chemistry confirm that the features of the “building blocks” – the fundamental structural components – produced by the biomineralization process were substantially unaffected by increased acidification. Furthermore, the pH up-regulation observed in this study could potentially explain the previous hypothesis that less “building blocks” are produced with increasing acidification ultimately leading to increased skeletal porosity and to reduced net calcification rate computed by including the total volume of the pore space. In fact, assuming that the available energy at the three sites is the same, this energy at the low pH sites could be partitioned among fewer calicoblastic cells that consume more energy given the larger difference between external and internal pH compared to the control, leading to the production of less building blocks (i.e., formation of pores inside the skeleton structure, determining increased porosity). However, we cannot exclude that also dissolution may play a role in increasing porosity. Thus, the ability of scleractinian corals to maintain elevated pHcf relative to ambient seawater might not always be sufficient to counteract declines in net calcification under OA scenarios.