scholarly journals New Insights on the Diurnal Mechanism of Calcification in the Stony Coral, Stylophora pistillata

2022 ◽  
Vol 8 ◽  
Author(s):  
Maayan Neder ◽  
Raoul Saar ◽  
Assaf Malik ◽  
Gilad Antler ◽  
Tali Mass

Scleractinian corals are evolutionary-successful calcifying marine organisms, which utilize an endo-symbiotic relationship with photosynthetic dinoflagellate algae that supply energy products to their coral hosts. This energy further supports a higher calcification rate during the day in a process known as light enhanced calcification. Although this process has been studied for decades, the mechanisms behind it are still unknown. However, photosynthesis and respiration also cause daily fluctuations in oxygen and pH levels, resulting in the coral facing highly variable conditions. Here we correlated gene expression patterns with the physiological differences along the diel cycle to provide new insights on the daily dynamic processes, including circadian rhythm, calcification, symbiosis, cellular arrangement, metabolism, and energy budget. During daytime, when solar radiation levels are highest, we observed increased calcification rate combined with an extensive up-regulation of genes associated with reactive oxygen species, redox, metabolism, ion transporters, skeletal organic matrix, and mineral formation. During the night, we observed a vast shift toward up-regulation of genes associated with cilia movement, tissue development, cellular movement, antioxidants, protein synthesis, and skeletal organic matrix formation. Our results suggest that light enhanced calcification is related to several processes that occur across the diel cycle; during nighttime, tissue might elevate away from the skeleton, extending the calcifying space area to enable the formation of a new organic framework template. During daytime, the combination of synthesis of acid-rich proteins and a greater flux of ions to the sites of calcification facilitate the conditions for extensive mineral growth.

1998 ◽  
Vol 201 (13) ◽  
pp. 2001-2009 ◽  
Author(s):  
D Allemand ◽  
É Tambutté ◽  
JP Girard ◽  
J Jaubert

The kinetics of organic matrix biosynthesis and incorporation into scleractinian coral skeleton was studied using microcolonies of Stylophora pistillata. [14C]Aspartic acid was used to label the organic matrix since this acidic amino acid can represent up to 50 mol % of organic matrix proteins. External aspartate was rapidly incorporated into tissue protein without any detectable lag phase, suggesting either a small intracellular pool of aspartic acid or a pool with a fast turn-over rate. The incorporation of 14C-labelled macromolecules into the skeleton was linear over time, after an initial delay of 20 min. Rates of calcification, measured by the incorporation of 45Ca into the skeleton, and of organic matrix biosynthesis and incorporation into the skeleton were constant. Inhibition of calcification by the Ca2+ channel inhibitor verapamil reduced the incorporation of organic matrix proteins into the skeleton. Similarly, organic matrix incorporation into the skeleton, but not protein synthesis for incorporation into the tissue compartment, was dependent on the state of polymerization of both actin and tubulin, as shown by the sensitivity of this process to cytochalasin B and colchicin. These drugs may inhibit exocytosis of organic matrix proteins into the subcalicoblastic space. Finally, inhibition of protein synthesis by emetin or cycloheximide and inhibition of N-glycosylation by tunicamycin reduced both the incorporation of macromolecules into the skeleton and the rate of calcification. This suggests that organic matrix biosynthesis and its migration towards the site of calcification may be a prerequisite step in the calcification process. On the basis of these results, we investigated the effects of tributyltin (TBT), a component of antifouling painting known to interfere with biomineralization processes. Our results have shown that this xenobiotic significantly inhibits protein synthesis and the subsequent incorporation of protein into coral skeleton. This effect was correlated with a reduction in the rate of calcification. Protein synthesis was shown to be the parameter most sensitive to TBT (IC50=0.2 micromol l-1), followed by aspartic acid uptake by coral tissue (IC50=0.6 micromol l-1), skeletogenesis (IC50=3 micromol l-1) and Ca2+ uptake by coral tissue (IC50=20 micromol l-1). These results suggest that the mode of action of TBT on calcification may be the inhibition of organic matrix biosynthesis.


PeerJ ◽  
2016 ◽  
Vol 4 ◽  
pp. e1814 ◽  
Author(s):  
Keren Maor-Landaw ◽  
Oren Levy

It is well-established that there is a hierarchy of susceptibilities amongst coral genera during heat-stress. However, molecular mechanisms governing these differences are still poorly understood. Here we explored if specific corals possessing different morphologies and different susceptibilities to heat stress may manifest varied gene expression patterns. We examined expression patterns of seven genes in the branching coralsStylophora pistillataandAcropora eurystomaand additionally in the massive robust coral,Poritessp. The tested genes are representatives of key cellular processes occurring during heat-stress in Cnidaria: oxidative stress, ER stress, energy metabolism, DNA repair and apoptosis. Varied response to the heat-stress, in terms of visual coral paling, algal maximum quantum yield and host gene expression was evident in the different growth forms. The two branching corals exhibited similar overall responses that differed from that of the massive coral.A. eurystomathat is considered as a susceptible species did not bleach in our experiment, but tissue sloughing was evident at 34 °C. Interestingly, in this species redox regulation genes were up-regulated at the very onset of the thermal challenge. InS. pistillata, bleaching was evident at 34 °C and most of the stress markers were already up-regulated at 32 °C, either remaining highly expressed or decreasing when temperatures reached 34 °C. The massivePoritesspecies displayed severe bleaching at 32 °C but stress marker genes were only significantly elevated at 34 °C. We postulate that by expelling the algal symbionts fromPoritestissues, oxidation damages are reduced and stress genes are activated only at a progressed stage. The differential gene expression responses exhibited here can be correlated with the literature well-documented hierarchy of susceptibilities amongst coral morphologies and genera in Eilat’s coral reef.


2019 ◽  
Vol 9 (1) ◽  
Author(s):  
C. Bernardet ◽  
E. Tambutté ◽  
N. Techer ◽  
S. Tambutté ◽  
A. A. Venn

AbstractCoral calcification underpins biodiverse reef ecosystems, but the physiology underlying the thermal sensitivity of corals to changing seawater temperatures remains unclear. Furthermore, light is also a key factor in modulating calcification rates, but a mechanistic understanding of how light interacts with temperature to affect coral calcification is lacking. Here, we characterized the thermal performance curve (TPC) of calcification of the wide-spread, model coral species Stylophora pistillata, and used gene expression analysis to investigate the role of ion transport mechanisms in thermally-driven declines in day and nighttime calcification. Focusing on genes linked to transport of dissolved inorganic carbon (DIC), calcium and H+, our study reveals a high degree of coherence between physiological responses (e.g. calcification and respiration) with distinct gene expression patterns to the different temperatures in day and night conditions. At low temperatures, calcification and gene expression linked to DIC transport processes were downregulated, but showed little response to light. By contrast, at elevated temperature, light had a positive effect on calcification and stimulated a more functionally diverse gene expression response of ion transporters. Overall, our findings highlight the role of mechanisms linked to DIC, calcium and H+ transport in the thermal sensitivity of coral calcification and how this sensitivity is influenced by light.


1993 ◽  
Vol 4 (5) ◽  
pp. 679-728 ◽  
Author(s):  
Anders Linde ◽  
Michel Goldberg

The formation of dentin, dentinogenesis, comprises a sophisticated interplay between several factors in the tissue, cellular as well as extracellular. Dentin may be regarded as a calcified connective tissue. In this respect, as well as in its mode of formation, it is closely related to bone. Using dentinogenesis as an experimental model to study biomineralization provides several practical advantages, and the results may be extrapolated to understand similar processes in other tissues, primarily bone. After describing dentin structure and composition, this review discusses items such as the morphology of dentinogenesis; the dentinogenically active odontoblast, transport, and concentrations of mineral ions; the constituents of the dentin organic matrix; and the presumed mechanisms involved in mineral formation.


2013 ◽  
Vol 110 (10) ◽  
pp. 3788-3793 ◽  
Author(s):  
J. L. Drake ◽  
T. Mass ◽  
L. Haramaty ◽  
E. Zelzion ◽  
D. Bhattacharya ◽  
...  

2000 ◽  
Vol 6 (S2) ◽  
pp. 1070-1071
Author(s):  
Guofeng Xu ◽  
Nan Yao ◽  
Ilhan A. Aksay ◽  
John T. Groves

Exquisite control over the morphology of inorganic materials is well demonstrated in biological mineralization. An elegant example is the mulluscan nacre, in which aragonite (a polymorph of calcium carbonate) forms as thin films of about 0.5|im thick between organic matrices as a result of an interplay between templating and inhibition (Figure 1). Not surprising, biomineralization has inspired many recent research efforts in biomimetic materials synthesis, especially the synthesis of inorganic thin films. The majority of these efforts have exclusively focused on exploring the promoting effect on mineral formation by templates. A major drawback of this approach is the lack of control over the mineral growth in the direction normal to the template, which often leads to the formation of discrete patches instead of a true film. In this report, we describe a strategy which takes advantage of the interplay between templating and inhibiting, as utilized by organisms, to synthesize macroscopic and continuous CaCO3 thin films.


2016 ◽  
Vol 283 (1829) ◽  
pp. 20160322 ◽  
Author(s):  
Tali Mass ◽  
Hollie M. Putnam ◽  
Jeana L. Drake ◽  
Ehud Zelzion ◽  
Ruth D. Gates ◽  
...  

Reef-building corals begin as non-calcifying larvae that, upon settling, rapidly begin to accrete skeleton and a protein-rich skeletal organic matrix that attach them to the reef. Here, we characterized the temporal and spatial expression pattern of a suite of biomineralization genes during three stages of larval development in the reef-building coral Pocillopora damicornis : stage I, newly released; stage II, oral-aborally compressed and stage III, settled and calcifying spat. Transcriptome analysis revealed 3882 differentially expressed genes that clustered into four distinctly different patterns of expression change across the three developmental stages. Immunolocalization analysis further reveals the spatial arrangement of coral acid-rich proteins (CARPs) in the overall architecture of the emerging skeleton. These results provide the first analysis of the timing of the biomineralization ‘toolkit’ in the early life history of a stony coral.


2020 ◽  
Author(s):  
Laura Capasso ◽  
Philippe Ganot ◽  
Víctor Planas-Bielsa ◽  
Sylvie Tambutté ◽  
Didier Zoccola

Abstract Background: Reef-building corals regularly experience changes in intra and extracellular H+ concentration ([H+]) due to physiological and environmental processes. Stringent control of [H+] is required for the maintenance of homeostatic acid-base balance in coral cells and is achieved through the regulation of intracellular pH (pHi). This task is especially challenging for reef-building corals that share an endosymbiotic relationship with photosynthetic dinoflagellates (family Symbiodinaceae), which exert a significant effect on the pHi of coral cells. Despite their importance, the pH regulatory proteins involved in the homeostatic acid-base balance have been scarcely investigated in corals. Here, we reported the full characterisation in terms of genomic structure, domain topology and phylogeny of three majors H+ transporter families implicated in pHi regulation; we investigated their tissue-specific expression and we assessed the effect of seawater acidification on their level of expression.Results: We identified members of the Na+/H+ exchanger (SLC9), vacuolar-type electrogenic H+-ATP hydrolases (V-ATPase) and voltage-gated proton channels (HvCN) families in the genome and transcriptome of S. pistillata. In addition, we identified a novel member of the HvCN gene family in the cnidarian subclass Hexacorallia, which has never been described in any species to date. We also reported key residues that participate to the H+ transporters substrate specificity, protein function and regulation. Lastly, we demonstrated that some of these have different tissue expression patterns and are mostly unaffected by exposure to seawater acidification.Conclusions: In this study, we provide the first characterization of the H+ transporters genes that contribute to homeostatic acid-base balance in coral cells. This work will enrich knowledge about basic aspects of coral biology, bearing important implications for our understanding of how corals regulate their intracellular environment.


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