The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals
Abstract Background The process of calcium carbonate biomineralization has arisen multiple times during metazoan evolution. In the phylum Cnidaria, biomineralization has mostly been studied in the subclass Hexacorallia (i.e. stony corals) in comparison to the subclass Octocorallia (i.e. red corals);...
| Main Authors: | , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
BMC
2021-01-01
|
| Series: | BMC Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1186/s12862-020-01734-0 |
| _version_ | 1818681864979742720 |
|---|---|
| author | Nathalie Le Roy Philippe Ganot Manuel Aranda Denis Allemand Sylvie Tambutté |
| author_facet | Nathalie Le Roy Philippe Ganot Manuel Aranda Denis Allemand Sylvie Tambutté |
| author_sort | Nathalie Le Roy |
| collection | DOAJ |
| description | Abstract Background The process of calcium carbonate biomineralization has arisen multiple times during metazoan evolution. In the phylum Cnidaria, biomineralization has mostly been studied in the subclass Hexacorallia (i.e. stony corals) in comparison to the subclass Octocorallia (i.e. red corals); the two diverged approximately 600 million years ago. The precious Mediterranean red coral, Corallium rubrum, is an octocorallian species, which produces two distinct high-magnesium calcite biominerals, the axial skeleton and the sclerites. In order to gain insight into the red coral biomineralization process and cnidarian biomineralization evolution, we studied the protein repertoire forming the organic matrix (OM) of its two biominerals. Results We combined High-Resolution Mass Spectrometry and transcriptome analysis to study the OM composition of the axial skeleton and the sclerites. We identified a total of 102 OM proteins, 52 are found in the two red coral biominerals with scleritin being the most abundant protein in each fraction. Contrary to reef building corals, the red coral organic matrix possesses a large number of collagen-like proteins. Agrin-like glycoproteins and proteins with sugar-binding domains are also predominant. Twenty-seven and 23 proteins were uniquely assigned to the axial skeleton and the sclerites, respectively. The inferred regulatory function of these OM proteins suggests that the difference between the two biominerals is due to the modeling of the matrix network, rather than the presence of specific structural components. At least one OM component could have been horizontally transferred from prokaryotes early during Octocorallia evolution. Conclusion Our results suggest that calcification of the red coral axial skeleton likely represents a secondary calcification of an ancestral gorgonian horny axis. In addition, the comparison with stony coral skeletomes highlighted the low proportion of similar proteins between the biomineral OMs of hexacorallian and octocorallian corals, suggesting an independent acquisition of calcification in anthozoans. |
| first_indexed | 2024-12-17T10:09:44Z |
| format | Article |
| id | doaj.art-e6dd0bf9b50246d5bafe6d4a273d6839 |
| institution | Directory Open Access Journal |
| issn | 2730-7182 |
| language | English |
| last_indexed | 2024-12-17T10:09:44Z |
| publishDate | 2021-01-01 |
| publisher | BMC |
| record_format | Article |
| series | BMC Ecology and Evolution |
| spelling | doaj.art-e6dd0bf9b50246d5bafe6d4a273d68392022-12-21T21:53:04ZengBMCBMC Ecology and Evolution2730-71822021-01-0121112110.1186/s12862-020-01734-0The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocoralsNathalie Le Roy0Philippe Ganot1Manuel Aranda2Denis Allemand3Sylvie Tambutté4Centre Scientifique de MonacoCentre Scientifique de MonacoRed Sea Research Center, King Abdullah University of Science and Technology (KAUST)Centre Scientifique de MonacoCentre Scientifique de MonacoAbstract Background The process of calcium carbonate biomineralization has arisen multiple times during metazoan evolution. In the phylum Cnidaria, biomineralization has mostly been studied in the subclass Hexacorallia (i.e. stony corals) in comparison to the subclass Octocorallia (i.e. red corals); the two diverged approximately 600 million years ago. The precious Mediterranean red coral, Corallium rubrum, is an octocorallian species, which produces two distinct high-magnesium calcite biominerals, the axial skeleton and the sclerites. In order to gain insight into the red coral biomineralization process and cnidarian biomineralization evolution, we studied the protein repertoire forming the organic matrix (OM) of its two biominerals. Results We combined High-Resolution Mass Spectrometry and transcriptome analysis to study the OM composition of the axial skeleton and the sclerites. We identified a total of 102 OM proteins, 52 are found in the two red coral biominerals with scleritin being the most abundant protein in each fraction. Contrary to reef building corals, the red coral organic matrix possesses a large number of collagen-like proteins. Agrin-like glycoproteins and proteins with sugar-binding domains are also predominant. Twenty-seven and 23 proteins were uniquely assigned to the axial skeleton and the sclerites, respectively. The inferred regulatory function of these OM proteins suggests that the difference between the two biominerals is due to the modeling of the matrix network, rather than the presence of specific structural components. At least one OM component could have been horizontally transferred from prokaryotes early during Octocorallia evolution. Conclusion Our results suggest that calcification of the red coral axial skeleton likely represents a secondary calcification of an ancestral gorgonian horny axis. In addition, the comparison with stony coral skeletomes highlighted the low proportion of similar proteins between the biomineral OMs of hexacorallian and octocorallian corals, suggesting an independent acquisition of calcification in anthozoans.https://doi.org/10.1186/s12862-020-01734-0Corallium rubrumBiomineralizationAxial skeletonScleritesOrganic matrixProteomics |
| spellingShingle | Nathalie Le Roy Philippe Ganot Manuel Aranda Denis Allemand Sylvie Tambutté The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals BMC Ecology and Evolution Corallium rubrum Biomineralization Axial skeleton Sclerites Organic matrix Proteomics |
| title | The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| title_full | The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| title_fullStr | The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| title_full_unstemmed | The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| title_short | The skeletome of the red coral Corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| title_sort | skeletome of the red coral corallium rubrum indicates an independent evolution of biomineralization process in octocorals |
| topic | Corallium rubrum Biomineralization Axial skeleton Sclerites Organic matrix Proteomics |
| url | https://doi.org/10.1186/s12862-020-01734-0 |
| work_keys_str_mv | AT nathalieleroy theskeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT philippeganot theskeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT manuelaranda theskeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT denisallemand theskeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT sylvietambutte theskeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT nathalieleroy skeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT philippeganot skeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT manuelaranda skeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT denisallemand skeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals AT sylvietambutte skeletomeoftheredcoralcoralliumrubrumindicatesanindependentevolutionofbiomineralizationprocessinoctocorals |