The shell matrix and microstructure of the Ram's Horn squid: molecular and structural characterization

Oudot, Morgane, Neige, Pascal, Ben Shir, Ira, Schmidt, Asher, Strugnell, Jan M., Plasseraud, Laurent, Broussard, Cédric, Hoffmann, René, Lukeneder, Alexander, and Marin, Frédéric (2020) The shell matrix and microstructure of the Ram's Horn squid: molecular and structural characterization. Journal of Structural Biology, 211 (1). 107507.

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Abstract

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, the organic matrix. In spite of several studies, these components are mainly known for bivalves and gastropods. In the present study, we investigated the physical and biochemical properties of the internal planispiral shell of the Ram's Horn squid Spirula spirula. Scanning Electron Microscope investigations of the shell reveal a complex microstructural organization. The saccharides constitute a quantitatively important moiety of the matrix, as shown by Fourier-transform infrared and solid-state nuclear magnetic resonance spectroscopies. NMR identified beta-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insoluble matrices and in silico searches were performed, first on heterologous metazoans models, and secondly on an unpublished transcriptome of Spirula spirula.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, 39 hits were obtained, including transferrin, a serine protease inhibitor, matrilin, or different histones. 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 demonstrates that there is no obvious phylogenetic signal in the cephalopod skeletal matrix.

Item ID: 63800
Item Type: Article (Research - C1)
ISSN: 1095-8657
Keywords: Biomineralization, Shell, Ram's horn squid, Microstructure, Proteomic, Chitin
Copyright Information: © 2020 Elsevier Inc. All rights reserved.
Funders: CNRS, Israel Science Foundation (ISF)
Projects and Grants: CNRS-Interrvie project 'BECOME FREE', ISF grant 2001/17
Date Deposited: 08 Jul 2020 07:49
FoR Codes: 31 BIOLOGICAL SCIENCES > 3109 Zoology > 310911 Animal structure and function @ 70%
31 BIOLOGICAL SCIENCES > 3105 Genetics > 310505 Gene expression (incl. microarray and other genome-wide approaches) @ 30%
SEO Codes: 96 ENVIRONMENT > 9608 Flora, Fauna and Biodiversity > 960808 Marine Flora, Fauna and Biodiversity @ 100%
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