The argonaut constructs its shell via physical self-organization and coordinated cell sensorial activity. (A. Checa et al.)_Dataset.

Published: 17 September 2021| Version 2 | DOI: 10.17632/n37bddwy7k.2
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Description

The shell of the cephalopod Argonauta consists of two layers of fibers that elongate perpendicular to the shell surfaces. Fibers have a calcitic core sheathed by extremely thin organic membranes, which form a polygonal network in cross-section. During growth, fibers with small cross-sectional areas tend to shrink, whereas those with large sections tend to widen, i.e. they follow the von Neumann-Mullins law. We hypothesize that fibers evolve as an emulsion between the fluid precursors of both the mineral and organic phases. In addition, when polygons reach big cross-sectional areas, they become subdivided by new membranes. To interpret this partitioning process we infer that the living cells from the mineralizing tissue are able to ‘locate’ and subdivide particularly large polygons. To do this, living cells must perform contact recognition and subsequent secretion at sub-micron scale. Accordingly, the fabrication of the argonaut shell proceeds by physical self-organization together with direct cellular activity

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We analyze the evolution of the organo-mineral patterns throughout growth and try to assimilate them, whenever possible, to feasible physical processes, also taking into account the capabilities of the calcifying epithelial cells. We have applied this approach to the shell produced by females of the cephalopod Argonauta. Composition: First of all, X-ray diffraction (XRD) analysis indicates that calcite is the only mineral phase present. The results of the Rietveld analysis (Table S1) show well-defined changes in calcite unit cell parameters with respect to pure inorganic calcite. On the other hand, thermogravimetry analysis coupled with differential scanning calorimetry (TGA-DSC) revealed a ~1.5% of structural water (weight loss up to 200°C), and 8.68% of organic matter (weight loss between 200-600%), that is, a total of 11.91% of amorphous material, notably higher than the amount calculated by XRD. This indicates that XRD may not be sensitive enough to quantify all amorphous components. Fourier-transform infrared spectroscopy (FTIR) spectra of the organic fraction showed strong protein peaks (Amide I and Amide II) and low-intensity absorption peaks in the polysaccharide region, indicating a predominance of proteins, and is in agreement with previous results on the acid-insoluble matrix fraction of Argonauta hians. Shell structure and Microstructure: We have studied the 3D distribution of cavities by high-resolution techniques: SEM, TEM, and AFM combining the results of all these techniques: SEM observations reveal that the shell consists of two finely prismatic or fibrous layers separated by a central organic layer whilst TEM and atomic force microscopy (AFM) observations reveal that the calcite constituting the shell of Argonauta has an ultrastructure similar to that of most other calcium carbonate biominerals. Both AFM and TEM observations are consistent with the presence of a minor ACC component. Evolution of the organo-mineral pattern during growth: The study by focused ion beam coupled with SEM (FIB-SEM)-aided slice and view, allowed us to track the evolution of the organo-mineral network during growth. In this way, we could analyze the evolution of such cavities during growth. Based on the observed topology, we infer that the animal creates an emulsion at the interface between the mineralized shell and the living tissue, at the same time that the shell-secreting epithelium cells are capable of ‘sense’ the organo-mineral pattern and react accordingly, by both continuing the pattern and subdividing particularly large cavities. In this way, we develop a fabricational model able to explain shell formation by physical self-organization together with a finely orchestrated cell behavior.