Molecular Cloning and Characterization of First Organic Matrix Protein from Sclerites of Red Coral, Corallium rubrum

Debreuil, Julien; Tambutté, Éric; Zoccola, Didier; Deleury, Emeline; Guigonis, Jean-Marie; Samson, Michel; Allemand, Denis; Tambutté, Sylvie

doi:10.1074/jbc.m112.352005

Cited by 24 publications

(38 citation statements)

References 68 publications

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“…It has been noted in the introduction that the LacazeDuthiers's hypothesis for the formation of the C. rubrum entire skeleton is classically considered as a mere aggregation and cementing of sclerites (Allemand and Bénazet-Tambutté 1996;Bayer and Cairns 2003;Cuif et al 2011;Debreuil et al 2012;Weinberg 1976). As a matter of fact, Lacaze-Duthiers's opinion is more subtle and deserves further examination.…”

Section: Comparison To Previous Modelsmentioning

confidence: 99%

“…Thus, for Lacaze-Duthiers, sclerites play a role in the formation of the annular part (though not as important as in the central core). The presence of sclerites in the annular part has been challenged by Allemand and Bénazet-Tambutté (1996), Allemand and Grillo (1992), Debreuil et al (2012Debreuil et al ( , 2011aDebreuil et al ( , 2011b, and Grillo et al (1993) who concluded that the growth of annular part of the skeleton does not involve sclerites. This conclusion was reached in part on the basis of biocalcification kinetic experiments indicating that there was no delay in the calcification of sclerites and annular skeleton as would be expected if the skeleton was made by a process of sclerite aggregation (Allemand and Grillo 1992).…”

Section: Comparison To Previous Modelsmentioning

confidence: 99%

See 1 more Smart Citation

Block-by-block and layer-by-layer growth modes in coral skeletons

Perrin

Vielzeuf

Ricolleau

et al. 2015

American Mineralogist

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Understanding the dynamics of biomineral growth is a challenging goal of biomineralogy that can be achieved in part by deciphering biomineral structures and chemistries. The morphology, structure, and chemistry of six skeletons of Corallium and Paracorallium species (C. rubrum, C. elatius, C. johnsoni, C. niobe, P. japonicum, and P. thrinax) from the Mediterranean, the Atlantic, and the Pacific oceans have been studied by X-ray micro-computed tomography, polarized light microscope, scanning electron microscope, and electron microprobe. All species have two types of biomineral structures: an inner skeleton and sclerites that are small grains of Mg-calcite found in the living tissues surrounding the skeleton. All skeletons display a central core surrounded by an annular domain. In the species studied by electron microprobe (C. rubrum, C. elatius, and P. japonicum), the central core and the annular domains display different chemical compositions with the core richer in magnesium and poorer in sulfur than the annular domain. In terms of structure, special emphasis has been put on central cores for which little data are available. The central cores are made of sclerites and sclerite aggregates within a cement consisting of fine layers of Mg-calcite. On the other hand, the annular parts are made of fine concentric layers of calcite crystallites with only rare sclerites. These contrasting features imply two different growth modes: (1) a "block and cement" mode taking place at the apex of a branch and associated with a fast axial growth rate (~2 mm/yr); and (2) a layer-by-layer mode occurring below the apex and associated with a slow radial growth (~0.2 mm/yr). The change from a growth mode to another is anatomically controlled by the presence of a continuous network of gastrodermal canals around the sub-apical skeleton, preventing to a large extent the aggregation of sclerites. It is generally accepted that the Coralliidae family exhibits different types of skeletogeneses. In contrast with this idea, we observe that all studied Corallium species display remarkable similarities in terms of skeletogenesis and a unifying growth model for the Corallium genus is proposed. Similarities and differences with previous models are discussed. The present study shows that the morphological criterion initially used to establish the genus Paracorallium in the Coralliidae family is inadequate.

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Section: Comparison To Previous Modelsmentioning

confidence: 99%

Section: Comparison To Previous Modelsmentioning

confidence: 99%

Block-by-block and layer-by-layer growth modes in coral skeletons

Perrin

Vielzeuf

Ricolleau

et al. 2015

American Mineralogist

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“…On the contrary, the occurrence within Octocorallia of both calcite and aragonite skeletons offers a unique opportunity to compare the skeletogenic repertoires associated with different skeletal structures and CaCO 3 polymorphs. Despite this, information on octocoral biomineralization-related proteins is extremely limited (but see Debreuil et al (2012; and Rahman et al (2011) ), and transcriptomic-proteomic coupled data is hitherto not available for this group.…”

Section: Introductionmentioning

confidence: 99%

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

Conci

Lehmann

Vargas

et al. 2019

Preprint

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Corals are ecosystem engineers of the coral reefs, one of the most biodiverse but severely threatened marine ecosystems. The ability of corals to form the three dimensional structure of reefs depends on the precipitation of calcium carbonate under biologically control. However, the exact mechanisms underlying this biologically controlled biomineralization remain to be fully unelucidated, for example whether corals employ a different molecular machinery for the deposition of different calcium carbonate (CaCO 3 ) polymorphs (i.e., aragonite or calcite). Here we used tandem mass spectrometry (MS/MS) to compare skeletogenic proteins, i.e., the proteins occluded in the skeleton of three octocoral and one scleractinian species: Tubipora musica and Sinularia cf. cruciata , both forming calcite sclerites, the blue coral Heliopora coerulea with an aragonitic rigid skeleton, and the scleractinian aragonitic Montipora digitata . We observed extremely low overlap between aragonitic and calcitic species, while a core set of proteins is shared between octocorals producing calcite sclerites.However, the same carbonic anhydrase (CruCA4) is employed for the formation of skeletons of both polymorphs. Similarities could also be observed between octocorals and scleractinians, including the presence of a galaxin-like protein.Additionally, as in scleractinians, some octocoral skeletogenic proteins, such as acidic proteins and scleritin, appear to have been secondarily co-opted for calcification and likely derive from proteins playing different extracellular functions. In H. coerulea, co-option was characterized by aspartic acid-enrichment of proteins. This work represents the first attempt to identify the molecular basis underlying coral skeleton polymorph diversity, providing several new research targets and enabling both future functional and evolutionary studies aimed at elucidating the origin and evolution of biomineralization in corals.

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“…Only recently an approach combining proteomics with genomics was applied unveiling a set of partial and complete sequences of proteins in the skeleton of the hexacoral S. pistillata (Drake et al 2013). Prior to this study, only the full sequence of two SOMPs, galaxin from the scleractinian Galaxea fascicularis (Fukuda et al 2003), and scleritin from the octocoral Corallium rubrum (Debreuil et al 2012) were published and a number of other partial sequences from octocorals (Rahman and Isa 2005; Rahman et al 2005; Rahman, Isa, Takemura, et al 2006; Rahman, Isa, Uehara 2006) and scleractinians (Puverel et al 2005). …”

Section: Introductionmentioning

confidence: 99%

The Skeletal Proteome of the Coral Acropora millepora: The Evolution of Calcification by Co-Option and Domain Shuffling

Ramos-Silva

Kaandorp

Huisman

et al. 2013

Molecular Biology and Evolution

169

279

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In corals, biocalcification is a major function that may be drastically affected by ocean acidification (OA). Scleractinian corals grow by building up aragonitic exoskeletons that provide support and protection for soft tissues. Although this process has been extensively studied, the molecular basis of biocalcification is poorly understood. Notably lacking is a comprehensive catalog of the skeleton-occluded proteins—the skeletal organic matrix proteins (SOMPs) that are thought to regulate the mineral deposition. Using a combination of proteomics and transcriptomics, we report the first survey of such proteins in the staghorn coral Acropora millepora. The organic matrix (OM) extracted from the coral skeleton was analyzed by mass spectrometry and bioinformatics, enabling the identification of 36 SOMPs. These results provide novel insights into the molecular basis of coral calcification and the macroevolution of metazoan calcifying systems, whereas establishing a platform for studying the impact of OA at molecular level. Besides secreted proteins, extracellular regions of transmembrane proteins are also present, suggesting a close control of aragonite deposition by the calicoblastic epithelium. In addition to the expected SOMPs (Asp/Glu-rich, galaxins), the skeletal repertoire included several proteins containing known extracellular matrix domains. From an evolutionary perspective, the number of coral-specific proteins is low, many SOMPs having counterparts in the noncalcifying cnidarians. Extending the comparison with the skeletal OM proteomes of other metazoans allowed the identification of a pool of functional domains shared between phyla. These data suggest that co-option and domain shuffling may be general mechanisms by which the trait of calcification has evolved.

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Molecular Cloning and Characterization of First Organic Matrix Protein from Sclerites of Red Coral, Corallium rubrum

Cited by 24 publications

References 68 publications

Block-by-block and layer-by-layer growth modes in coral skeletons

Block-by-block and layer-by-layer growth modes in coral skeletons

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

The Skeletal Proteome of the Coral Acropora millepora: The Evolution of Calcification by Co-Option and Domain Shuffling

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