Differential gene expression in skeletal organic matrix proteins of scleractinian corals associated with mixed aragonite/calcite skeletons under low mMg/Ca conditions

Abstract

Although coral skeletons generally comprise aragonite crystals, changes in the molar Mg/Ca ratio (mMg/Ca) in seawater result in the incorporation of calcite crystals. The formation mechanism of aragonite and calcite crystals in the scleractinian coral Acropora tenuis was therefore investigated by RNA-seq analysis, using early growth stage calcite (mMg/Ca = 0.5) and aragonite (mMg/Ca = 5.2)-based corals. As a result, 1,287 genes were up-regulated and 748 down-regulated in calcite-based corals. In particular, sixty-eight skeletogenesis-related genes, such as ectin, galaxin, and skeletal aspartic acid-rich protein, were detected as up-regulated, and six genes, such as uncharacterized skeletal organic matrix protein 5, down-regulated, in low-Mg/Ca conditions. Since the number of down-regulated genes associated with the skeletal organic matrix of aragonite skeletons was much lower than that of up-regulated genes, it is thought that corals actively initiate construction of an aragonite skeleton by the skeletal organic matrix in low-Mg/Ca conditions. In addition, different types of skeletal organic matrix proteins, extracellular matrix proteins and calcium ion binding proteins appeared to change their expression in both calcite-formed and normal corals, suggesting that the composition of these proteins could be a key factor in the selective formation of aragonite or calcite CaCO3.

A modern scleractinian coral with a two-component calcite–aragonite skeleton

“…3 ), coinciding with the lowest ocean Mg/Ca ratio during the Phanerozoic (<1 mol/mol). Culturing experiments have suggested that low-Mg seawater chemistry strongly affects the expression of genes related to coral skeletal formation and may trigger a change from aragonite to calcite mineralogy ( 33 ). Other experiments have demonstrated a physiologically controlled calcite-to-aragonite mineralogical switch triggered by changes in the growth solution Mg/Ca ratio ( 21 , 34 , 35 ).…”

How corals made rocks through the ages

“…These proteins are secreted by the calicoblastic ectoderm (Puverel, Tambutté, Zoccola, et al, ; Yamashiro & Samata, ), serve to connect that cell layer to the pre‐existing skeleton (Clode & Marshall, , ), and pattern both the physical and chemical environment of the calcifying medium (Chen et al, ; Clode & Marshall, , ; Drake et al, ). The SOM allows coral aragonite precipitation even under calcite‐promoting conditions (Higuchi et al, ; Higuchi, Shirai, Mezaki, & Yuyama, ; Yuyama & Higuchi, ). The amino acid composition of the SOM proteins across Scleractinia is heavily biased toward aspartic and glutamic acids (Mass et al, ; Mitterer, ; Young, ), a phenomenon not observed for tissue protein complexes (Yamashiro & Samata, ).…”

“…1.5 to 5.2 mol/mol (Stolarski et al, ) and aragonite is still detected among calcite in modern Acropora spp. when reared at Mg/Ca = 0.5 mol/mol (Higuchi et al, , ; Yuyama & Higuchi, ). Furthermore, calcite‐promoting conditions in the Cretaceous seas (the lowest Mg/Ca in the Phanerozoic) did not dictate the CaCO 3 polymorph change in skeletons of corals that remained aragonitic through their entire fossil record (Janiszewska, Mazur, Escrig, Meibom, & Stolarski, ).…”

Molecular and mineral responses of corals grown under artificial Calcite Sea conditions

“…These observations were later corroborated by Higuchi et al (2014), who reported significant amounts of calcite in the skeleton of juvenile Acropora tenuis , albeit at lower m Mg: m Ca ratios compared to Ries (2006). More recently, Yuyama et al (2019) reported changes in gene expression in the scleractinian coral A. tenuis grown in Mg-depleted seawater. These included the up-regulation of several putative skeletogenic genes, suggesting that lower m Mg: m Ca elicits a response in the corals’ calcification machinery.…”

“…These included the up-regulation of several putative skeletogenic genes, suggesting that lower m Mg: m Ca elicits a response in the corals’ calcification machinery. However, since Yuyama et al (2019) only manipulated the Mg-content of the water leaving the calcium levels constant, the molecular response of corals to m Mg: m Ca ratios comparable to those observed during geological periods corresponding to Calcite Seas, when both the concentration of calcium and magnesium changed, remain unknown.…”