Stepwise Evolution of Coral Biomineralization Revealed with Genome-Wide Proteomics and Transcriptomics

Abstract

Despite the importance of stony corals in many research fields related to global issues, such as marine ecology, climate change, paleoclimatogy, and metazoan evolution, very little is known about the evolutionary origin of coral skeleton formation. In order to investigate the evolution of coral biomineralization, we have identified skeletal organic matrix proteins (SOMPs) in the skeletal proteome of the scleractinian coral, Acropora digitifera, for which large genomic and transcriptomic datasets are available. Scrupulous gene annotation was conducted based on comparisons of functional domain structures among metazoans. We found that SOMPs include not only coral-specific proteins, but also protein families that are widely conserved among cnidarians and other metazoans. We also identified several conserved transmembrane proteins in the skeletal proteome. Gene expression analysis revealed that expression of these conserved genes continues throughout development. Therefore, these genes are involved not only skeleton formation, but also in basic cellular functions, such as cell-cell interaction and signaling. On the other hand, genes encoding coral-specific proteins, including extracellular matrix domain-containing proteins, galaxins, and acidic proteins, were prominently expressed in post-settlement stages, indicating their role in skeleton formation. Taken together, the process of coral skeleton formation is hypothesized as: 1) formation of initial extracellular matrix between epithelial cells and substrate, employing pre-existing transmembrane proteins; 2) additional extracellular matrix formation using novel proteins that have emerged by domain shuffling and rapid molecular evolution and; 3) calcification controlled by coral-specific SOMPs.

An aposymbiotic primary coral polyp counteracts acidification by active pH regulation

“…1g: ROI 2 and 4, red arrows), after which the pH increased within 30 min. We cannot explain this phenomenon, but we speculate that primary polyps temporarily stopped the alkalization of pH SCM or discharged acidic compounds3232425 (such as coral acid-rich proteins) into the SCMs.…”

The skeletal proteome of the sea star Patiria miniata and evolution of biomineralization in echinoderms

“…Similar proteins are found in vertebrate bone proteomes [16–18] and proteins with Lrp domains have now been identified in coral mineral proteomes [31]. Genes encoding Lrp proteins have been implicated in human osteoporosis through genome-wide association studies [32, 33].…”

The Origin and Role of Organic Matrix in Coral Calcification: Insights From Comparing Coral Skeleton and Abiogenic Aragonite

“…First, organic matter coats aragonite crystals in the skeleton (Clode and Marshall, 2002), and elevated organic matter content is closely associated with the relatively disordered centers of calcification (COCs; also called "rapid accretion deposits" or RADs) (Benzerara et al, 2011;Falini et al, 2013;Von Euw et al, 2017). Second, organic molecules extracted from the skeleton have been attributed to certain roles in crystal growth (Constantz and Weiner, 1988;Weiner and Addadi, 1991;Allemand et al, 1998;Goldberg, 2001;Cuif et al, 2008;Reggi et al, 2014;Takeuchi et al, 2016), with some proteins even capable of inducing spontaneous aragonite precipitation from seawater . Finally, the unit cell of biogenic aragonite contracts after annealing (i.e., heating and allowing to cool), presumably due to the removal of the SOM from the lattice (Pokroy et al, 2004;Reggi et al, 2014;Zolotoyabko, 2017).…”