New Non-Bilaterian Transcriptomes Provide Novel Insights into the Evolution of Coral Skeletomes

Abstract

A general trend observed in animal skeletomes—the proteins occluded in animal skeletons—is the copresence of taxonomically widespread and lineage-specific proteins that actively regulate the biomineralization process. Among cnidarians, the skeletomes of scleractinian corals have been shown to follow this trend. However, distributions and phylogenetic analyses of biomineralization-related genes are often based on only a few species, with other anthozoan calcifiers such as octocorals (soft corals), not being fully considered. We de novo assembled the transcriptomes of four soft-coral species characterized by different calcification strategies (aragonite skeleton vs. calcitic sclerites) and data-mined published nonbilaterian transcriptome resources to construct a taxonomically comprehensive sequence database to map the distribution of scleractinian and octocoral skeletome components. Cnidaria shared no skeletome proteins with Placozoa or Ctenophora, but did share some skeletome proteins with Porifera, such as galaxin-related proteins. Within Scleractinia and Octocorallia, we expanded the distribution for several taxonomically restricted genes such as secreted acidic proteins, scleritin, and carbonic anhydrases, and propose an early, single biomineralization-recruitment event for galaxin sensu stricto. Additionally, we show that the enrichment of acidic residues within skeletogenic proteins did not occur at the Corallimorpharia–Scleractinia transition, but appears to be associated with protein secretion into the organic matrix. Finally, the distribution of octocoral calcification-related proteins appears independent of skeleton mineralogy (i.e., aragonite/calcite) with no differences in the proportion of shared skeletogenic proteins between scleractinians and aragonitic or calcitic octocorals. This points to skeletome homogeneity within but not between groups of calcifying cnidarians, although some proteins such as galaxins and SCRiP-3a could represent instances of commonality.

Comparative proteomics of octocoral and scleractinian skeletomes and the evolution of coral calcification

“…Nevertheless, the fact that only T. musica 's octo-galaxin 1 possess the endoprotease target motif characteristic of scleractinian skeletogenic galaxins (Fukuda et al 2003) , and that the observed polyphyly within galaxin phylogenies are likely affected by the inclusion of false homologs, sensitivity to analytical parameters, and aligning algorithms (Conci et al 2019) makes difficult to rule out the hypothesis of an ancient, biomineralization-related recruitment of (octo)galaxins prior to the divergence of octocorals from the remaining Anthozoa.…”

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

“…Common contaminants, potential symbiont, and bacterial sequences were filtered. Peptides were mapped against respective octocoral ( Conci et al. 2019) and M. digitata ( González-Pech et al.…”

Skeletons of Calcareous Benthic Hydroids (Medusozoa, Hydrozoa) under Ocean Acidification

“…According to an analysis of SOM homologs in cnidarians, including Hydrozoa, several proteins related to biomineralization were identified [38]. Extracellular adhesion proteins and carbonic anhydrases homologs were the most common proteins found (e.g., in Millepora alcicornis, Millepora complanata, and Millepora squarrosa).…”

“…Homolog proteins include enzymes such as peptidase-1 and peptidase-2 as well as acidic proteins like SAARP-1, SAARP-2, acidic SOMP, CARP4, CARP5, Integrin-like and two SAARP-like proteins; those proteins are involved in calcite formation [39]. Two galaxin ortholog proteins (Galaxin and Galaxin-2) [38] have been fully characterized by the calcifying matrix of scleractinian corals [40]. More interestingly, carbonic anhydrases, which are known to precipitate CaCO 3 in different calcareous organisms [41], have been identified in Hydrozoa species, CruCA-4, and Putative CA [38].…”

“…Two galaxin ortholog proteins (Galaxin and Galaxin-2) [38] have been fully characterized by the calcifying matrix of scleractinian corals [40]. More interestingly, carbonic anhydrases, which are known to precipitate CaCO 3 in different calcareous organisms [41], have been identified in Hydrozoa species, CruCA-4, and Putative CA [38]. Finally, in contrast to scleractinian corals, Hydrozoa species did not show small cysteine-rich proteins (SCRiPs) [38], whose function in corals is still unclear.…”