The shell matrix of the european thorny oyster, Spondylus gaederopus: microstructural and molecular characterization

• Published in: Journal of structural biology Vol. 211; no. 1; p. 107497
• Main Authors: Sakalauskaite, Jorune, Plasseraud, Laurent, Thomas, Jérôme, Albéric, Marie, Thoury, Mathieu, Perrin, Jonathan, Jamme, Frédéric, Broussard, Cédric, Demarchi, Beatrice, Marin, Frédéric
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 01.07.2020; Elsevier
• Subjects: Animal biology; Biochemistry, Molecular Biology; Biomineralization; Evolution; Invertebrate Zoology; Life Sciences; Liquid chromatography-tandem mass spectrometry; Proteomics; Shell biochemistry; Structural Biology; Biomineralization; Evolution; Liquid chromatography-tandem mass spectrometry; Shell biochemistry; Proteomics
• ISSN: 1047-8477; 1095-8657
• DOI: 10.1016/j.jsb.2020.107497

[Display omitted] •The first biomolecular characterization of Spondylus gaederopus shell.•Complex and peculiar shell microstructure, low in intracrystalline mineral-bound organics.•Shell proteome was analysed by high-resolution tandem mass spectrometry (LC-MS/MS).•Six shell proteins identified that represent a partial picture of Spondylus ‘shellome’.•Most sequences remain unknown and probably represent lineage-specific proteins. Molluscs, the largest marine phylum, display extraordinary shell diversity and sophisticated biomineral architectures. However, mineral-associated biomolecules involved in biomineralization are still poorly characterised. We report the first comprehensive structural and biomolecular study of Spondylus gaederopus, a pectinoid bivalve with a peculiar shell texture. Used since prehistoric times, this is the best-known shell of Europe’s cultural heritage. We find that Spondylus microstructure is very poor in mineral-bound organics, which are mostly intercrystalline and concentrated at the interface between structural layers. Using high-resolution liquid chromatography tandem mass spectrometry (LC-MS/MS) we characterized several shell protein fractions, isolated following different bleaching treatments. Several peptides were identified as well as six shell proteins, which display features and domains typically found in biomineralized tissues, including the prevalence of intrinsically disordered regions. It is very likely that these sequences only partially represent the full proteome of Spondylus, considering the lack of genomics data for this genus and the fact that most of the reconstructed peptides do not match with any known shell proteins, representing consequently lineage-specific sequences. This work sheds light onto the shell matrix involved in the biomineralization in spondylids. Our proteomics data suggest that Spondylus has evolved a shell-forming toolkit, distinct from that of other better studied pectinoids – fine-tuned to produce shell structures with high mechanical properties, while limited in organic content. This study therefore represents an important milestone for future studies on biomineralized skeletons and provides the first reference dataset for forthcoming molecular studies of Spondylus archaeological artifacts.