Molluscs are one of the most diversified phyla among metazoans. Most of them produce an external calcified shell, resulting from the secretory activity of a specialized epithelium of the calcifying mantle. This biomineralization process is controlled by a set of extracellular macromolecules, collectively defined as the organic matrix. In spite of several studies, these components are mainly known for bivalve and gastropod classes. In the present study, we investigated the physical and biochemical properties of the internal planispiral shell of the understudied Ram's Horn squid Spirula spirula (Cephalopoda, Decabrachia, Spirulida). Scanning Electron Microscope investigations of the shell reveal a complex microstructural organization, with septa sandwiched into the shell wall, in the form of a bevel. The saccharides constitute a quantitatively important moiety of the matrix, as shown by Fourier-transform infrared spectroscopy. Solid-state nuclear magnetic resonance spectroscopy identified β-chitin and additional polysaccharides, for a total amount of 80% of the insoluble fraction. Proteomics was applied to both soluble and insoluble matrices and in silico searches were performed, first on heterologous metazoans models, and secondly, on an unpublished transcriptome of Spirula spirula. In the first case, several peptides were identified, some of them matching with tyrosinase, chitinase 2, protease inhibitor, or immunoglobulin. In the second case, 38 hits were obtained, including transferrin, a serine protease inhibitor, matrilin, different histone-like, a 2-macroglobulin or a putative heme-binding/calcium-binding protein. The very few similarities with known molluscan shell matrix proteins suggest that Spirula spirula uses a unique set of shell matrix proteins for constructing its internal shell. The absence of similarity with closely related cephalopods such as the cuttlefish Sepia demonstrates that there is no obvious phylogenetic signal in the skeletal matrix of cephalopods.
Molluscs are known for their ability to produce a calcified shell resulting from a genetically controlled and matrix-mediated process, performed extracellularly. The occluded organic matrix consists of a complex mixture of proteins, glycoproteins and polysaccharides that are in most cases secreted by the mantle epithelium. To our knowledge, the model studied here—the argonaut, also called paper nautilus—represents the single mollusc example where this general scheme is not valid: the shell of this cephalopod is indeed formed by its first dorsal arms pair and it functions as an eggcase, secreted by females only; furthermore, this coiled structure is fully calcitic and the organization of its layered microstructures is unique. Thus, the argonautid shell appears as an apomorphy of this restricted family, not homologous to other cephalopod shells. In the present study, we investigated the physical and biochemical properties of the shell of Argonauta hians, the winged argonaut. We show that the shell matrix contains unusual proportions of soluble and insoluble components, and that it is mostly proteinaceous, with a low proportion of sugars that appear to be mostly sulfated glycosaminoglycans. Proteomics performed on different shell fractions generated several peptide sequences and identified a number of protein hits, not shared with other molluscan shell matrices. This may suggest the recruitment of unique molecular tools for mineralizing the argonaut’s shell, a finding that has some implications on the evolution of cephalopod shell matrices.
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