Different secretory repertoires control the biomineralization processes of prism and nacre deposition of the pearl oyster shell

Abstract

Mollusca evolutionary success can be attributed partly to their efficiency to sustain and protect their soft body with an external biomineralized structure, the shell. Current knowledge of the protein set responsible for the formation of the shell microstructural polymorphism and unique properties remains largely patchy. In Pinctada margaritifera and Pinctada maxima, we identified 80 shell matrix proteins, among which 66 are entirely unique. This is the only description of the whole "biomineralization toolkit" of the matrices that, at least in part, is thought to regulate the formation of the prismatic and nacreous shell layers in the pearl oysters. We unambiguously demonstrate that prisms and nacre are assembled from very different protein repertoires. This suggests that these layers do not derive from each other.mantle | mollusk shell matrix proteins | proteome | transcriptome | evolution

Deep conservation of bivalve nacre proteins highlighted by shell matrix proteomics of the Unionoida Elliptio complanata and Villosa lienosa

“…Our proteomic investigation also highlights the presence of a large set of 16 RLCD-containing proteins (electronic supplementary material, table S1) for which similar proteins (that are genuine orthologues for some of them) were previously observed in Pinctada nacre, namely MSI60-like, shematrin, G-,Q-, Y-, D-and M-rich proteins [2]. In addition, we identified new features such as a byssal protein-like, the homologues of which were detected some years ago in the byssus of the blue mussel [33].…”

“…The overall primary structure of shematrins is characterized by a signal peptide, G-G-Y-repeat motif, together with other more variable G-and Y-rich RLCDs and KKKY N-termini [36] that are also observed in this novel unionoid putative member. Shematrin-likes constitute one of the main SMP families, found in both the nacre and prismatic layer of the shell of Pinctada spp., and their corresponding transcripts are highly expressed in the mantle [2,20]. Surprisingly, their homologous sequences are missing from the Transcriptome Shotgun Assembly (TSA) databases of E. complanata and V. lienosa.…”

“…p and m exponents indicate that the protein was also detected in the prismatic shell layer of either Pinctada spp. or Mytilus spp., respectively [2,15,17,18]. (Online version in colour.)…”

“…Since the initial description of the primary structure of a mollusc shell protein in 1996 [15], numerous nacre-associated proteins have been described so far, mainly from three principal models: the pearl oyster [2,16] and the edible mussel for bivalves [17,18], and the abalone for gastropods [19]. Comparison of their respective nacre biomineralization toolkits from the pearl mussel Pinctada maxima and the abalone Haliotis asinina underlined unexpectedly very few sequence similarities, suggesting either that the bivalves and gastropods independently acquired the capacity to synthesize nacre or that these proteins present a rapid evolution rate, especially in abalone, leading to functional conservation of the respective nacre shell matrix protein sets with only limited primary structure similarities [20].…”

“…calcite and aragonite), generally assembled in superimposed CaCO 3 layers of different microstructures [1]. These different shell layer textures are produced under the control of specific extracellular matrices that are secreted by different zones of the external mantle epithelium [2]. These 'cell-free' matrices, which consist mainly of proteins, glycoproteins and polysaccharides, surround nascent CaCO 3 crystals and are incorporated into the shell crystalline architecture during growth.…”