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.
Highlights
Reef-building corals (Cnidaria, Anthozoa, Scleractinia) produce huge masses of calcium carbonate structures in the ocean [1]
Twelve skeletal organic matrix protein (SOMP) were conserved among three species, while fourteen proteins were shared between Acropora species but not found in S. pistillata
Four SOMPs of A. digitifera were not described in the proteome of the closely related A. millepora, while 12 SOMPs in the A. millepora proteome have not been detected in the A. digitifera skeleton
Summary
Reef-building corals (Cnidaria, Anthozoa, Scleractinia) produce huge masses of calcium carbonate structures in the ocean [1]. Coral reefs provide habitats for one-third of all described marine species [2]. Corals face a range of anthropogenic challenges, including. Loss of corals results in loss of entire reef ecosystems. Scleractinian corals, which appear in the fossil record as early as the Triassic [4,5,6], are the dominant reef builders in shallow tropical and subtropical oceans. Coral calcification is a striking example of biomineralization, a complicated process including crystal nucleation and crystal growth. The enigma is how corals regulate such an intricate process and how such a versatile mechanism arose
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