The evolution and future of carbonate precipitation in marine invertebrates: Witnessing extinction or documenting resilience in the Anthropocene?

Morphological and phylogenetic analyses suggest that the ability to precipitate carbonates evolved several times in marine invertebrates in the past 600 million years. Over the past decade, there has been a profusion of genomic, transcriptomic, and proteomic analyses of calcifying representatives from three metazoan phyla: Cnidaria, Echinodermata, and Mollusca. Based on this information, we compared proteins intimately associated with precipitated calcium carbonate in these three phyla. Specifically, we used a cluster analysis and gene ontology approach to compare ∼1500 proteins, from over 100 studies, extracted from calcium carbonates in stony corals, in bivalve and gastropod mollusks, and in adult and larval sea urchins to identify common motifs and differences. Our analysis suggests that there are few sequence similarities across all three phyla, supporting the independent evolution of biomineralization. However, there are core sets of conserved motifs in all three phyla we examined. These motifs include acidic proteins that appear to be responsible for the nucleation reaction as well as inhibition; structural and adhesion proteins that determine spatial patterning; and signaling proteins that modify enzymatic activities. Based on this analysis and the fossil record, we propose that biomineralization is an extremely robust and highly controlled process in metazoans that can withstand extremes in pH predicted for the coming century, similar to their persistence through the Paleocene-Eocene Thermal Maximum (∼55 Mya).