The Evolution of Calcification in Reef-Building Corals

Abstract

Corals build the structural foundation of coral reefs, one of the most diverse and productive ecosystems on our planet. Although the process of coral calcification that allows corals to build these immense structures has been extensively investigated, we still know little about the evolutionary processes that allowed the soft-bodied ancestor of corals to become the ecosystem builders they are today. Using a combination of phylogenomics, proteomics, and immunohistochemistry, we show that scleractinian corals likely acquired the ability to calcify sometime between ∼308 and ∼265 Ma through a combination of lineage-specific gene duplications and the co-option of existing genes to the calcification process. Our results suggest that coral calcification did not require extensive evolutionary changes, but rather few coral-specific gene duplications and a series of small, gradual optimizations of ancestral proteins and their co-option to the calcification process.

Keywords: biomineralization; calcium carbonate skeleton; coral reefs; phylogenomics.

Fig. 1.

Phylogenetic divergence across seven published cnidarian genomes. (a) Phylogenetic analysis of seven cnidarian genomes. The values on nodes indicate the posterior and mean node age. Values on branches show the age range (95% HPD). (b) Marginal density of divergence times for three groups, including Scleractinia, Corallimorpharia and Actiniaria. (c) Density of pair-wise genetic divergence between two scleractinians and two corallimorpharians calculated based on synonymous substitution rated (Ks) across 1,421 orthologous genes.

Fig. 2.

Plasma membrane calcium ATPase (PMCA). (a) Phylogeny of PMCA orthologs across hexacorallian genomes. (b) Expression of PMCA orthologs across six genomes. (c) Synteny of PMCA orthologs. (d) Immunolocalization of PMCA1, PMCA2, and PMCA3 in S. pistillata, E. pallida, Discosoma sp., and A. fenestrafer. AEnd, aboral endoderm; AEct, aboral ectoderm; CEct, calicoblastic ectoderm; Co, coelenteron; SK, skeleton.

Fig. 3.

Solute carrier 4. (a) Phylogeny of SLC4 across six hexacorallian genomes. (b) SLC4β, SLC4γ, and their surrounding genomic locus across six hexacorallian genomes. (c) Immunolocalization of SLC4β (left) and SLC4γ (right, published by Zoccola et al. 2015) in S. pistillata. AEnd, aboral endoderm; CEct, calicoblastic ectoderm; Co, coelenteron; SK, skeleton.

Fig. 4.

Carbonic anhydrases. (a) Phylogeny of CAs across six hexacorallians. Orange labels represent extracellular CAs, and blue labels represent intracellular CAs. (b) Expression of CAs across homologs in Scleractinia. Orange labels represent the extracellular CAs, and blue labels represent intracellular CAs. (c) Expression of CAs in different developmental stages of A. digitifera.

Fig. 5.

Comparison of the SOMPs identified in four proteomic studies.

Fig. 6.

Coral acid-rich proteins (CARPs). (a) Phylogenetic analysis of CARP4. (b) The abundance of aspartic and glutamic acid residues across the different homologs of CARP4s.