Comparative Proteomics of Octocoral and Scleractinian Skeletomes and the Evolution of Coral Calcification

Corals are the ecosystem engineers of coral reefs, one of the most biodiverse marine ecosystems. The ability of corals to form reefs depends on the precipitation of calcium carbonate (CaCO3) under biological control. However, several mechanisms underlying coral biomineralization remain elusive, for example, whether corals employ different molecular machineries to deposit different CaCO3 polymorphs (i.e., aragonite or calcite). Here, we used tandem mass spectrometry (MS/MS) to compare the proteins occluded in the skeleton of three octocoral and one scleractinian species: Tubipora musica and Sinularia cf. cruciata (calcite sclerites), the blue coral Heliopora coerulea (aragonitic skeleton), and the scleractinian aragonitic Montipora digitata. Reciprocal Blast analysis revealed extremely low overlap between aragonitic and calcitic species, while a core set of proteins is shared between octocorals producing calcite sclerites. However, the carbonic anhydrase CruCA4 is present in the skeletons of both polymorphs. Phylogenetic analysis highlighted several possible instances of protein co-option in octocorals. These include acidic proteins and scleritin, which appear to have been secondarily recruited for calcification and likely derive from proteins playing different functions. Similarities between octocorals and scleractinians included presence of a galaxin-related protein, carbonic anhydrases, and one hephaestin-like protein. Although the first two appear to have been independently recruited, the third appear to share a common origin. This work represents the first attempt to identify and compare proteins associated with coral skeleton polymorph diversity, providing several new research targets and enabling both future functional and evolutionary studies aimed at elucidating the origin and evolution of coral biomineralization.