A Nature’s Curiosity: The Argonaut “Shell” and Its Organic Content

Abstract

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.

Independent adoptions of a set of proteins found in the matrix of the mineralized shell-like eggcase of Argonaut octopuses

“…Within the five families of the incirrate octopuses, only the argonauts (Argonautidae) exceptionally have a calcified external shell-like structure (an "eggcase") which resembles the coiled shell of the Nautilids and Ammonoids (or, like a hollyhock leaf when folded in the that, at the first glance, the eggcase of the Argonauts appears morphologically similar to the biomineralized external shell of the Conchiferans, but they are microstructurally different (Oudot et al 2020b). The eggcase of the Argonauts contains only calcite crystals while the outer shell of molluscs contains mainly aragonite and calcite Mitchell et al 1994;Nixon and Young 2003;Saul and Stadum 2005).…”

The ‘Shellome’ of the Crocus Clam Tridacna crocea Emphasizes Essential Components of Mollusk Shell Biomineralization

“…DSL, the second most reactive lectin, marks the presence of monomers/oligomers of N -acetylglucosamine, suggesting that soluble derived products of chitin are present in the ASM. We suppose that the release of such soluble components ensue from the partial hydrolysis and solubilization of chitin by bleach, similarly to what occurs in a chitin-rich biomineral ( Oudot et al, 2020 ). This also suggests that chitin - accessible to bleach – is intercrystalline .…”

“…Our results obtained by two different techniques (HPAE-PAD and ELLA) confirms this latter finding: the presence of chitin in a 'non-pteriomorph, ' crossed-lamellar bivalve model, where it is believed to participate -via the formation of chitin-protein complexes -to the 3D-structuring of the organic framework. Recent data (Agbaje et al, 2018;Oudot et al, 2020) show that chitin, which importance in shell formation is commonly admitted, is not universally distributed in this exoskeleton. Understanding its exact role in mineral deposition, analyzing its distribution and abundance across the Mollusca and detecting which polymer replaced it functionally in chitin-less shells are major evolutionary questions that deserve attention.…”

Biominerals: Formation, Function, Properties

“…Biocarbonate mineralization is the focus of research described by Oudot et al [7] and Mishima et al [8]. The calcitic shell of Argonauta hians was sampled for biochemical characterization of the extracellular organic matrix present in the shell [7].…”

“…Biocarbonate mineralization is the focus of research described by Oudot et al [7] and Mishima et al [8]. The calcitic shell of Argonauta hians was sampled for biochemical characterization of the extracellular organic matrix present in the shell [7]. The results show that the latter consists of unusual proportions of soluble and insoluble components and consists mainly of proteins complemented with a low amount of sulphated glycosaminoglycans.…”