Stepwise Evolution of Coral Biomineralization Revealed with Genome-Wide Proteomics and Transcriptomics

PLoS One. 2016 Jun 2;11(6):e0156424. doi: 10.1371/journal.pone.0156424. eCollection 2016.

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.

MeSH terms

  • Animals
  • Anthozoa / genetics*
  • Calcification, Physiologic / genetics
  • Calcium Carbonate / metabolism
  • Climate Change
  • Evolution, Molecular*
  • Genome
  • Proteome / genetics*
  • Transcriptome / genetics*

Substances

  • Proteome
  • Calcium Carbonate

Grants and funding

Japan Society for the Promotion of Science KAKENHI (https://www.jsps.go.jp/english/index.html, 24241071 and 25660172) and The Canon Foundation (http://www.canonfoundation.org/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.