Multi-omics analysis of the shell proteins in two bivalves reveals the core elements of the biomineralization toolkit

ABSTRACT: Mollusks produce calcified shells with vast diversity in morphology and microstructure, which is vital for their survival and holds promise for novel bioinspired material synthesis. Shell proteins embedded in minerals are the key to understanding the exquisite control of shell mineralization. In the past decade, high-throughput multi-omics assay has yielded the identification of a large number of shell proteins. However, how these proteins assemble into shell matrices and guide the precipitation of the CaCO3 in a highly controlled manner is still unclear. In this study, we coupled transcriptomic and proteomic analysis to identify shell proteins from the highly conserved myostracum layer in the pen shell Atrina pectinata and the Pacific oyster Crassostrea gigas and compared the shell proteins to the nascent shell layers. As a result, we characterized two main groups of shell proteins, namely the chitin-related and tyrosine oxidation-related proteins, representing the highly conserved core elements of biomineralization toolkit in molluscs. Moreover, we developed a new screening assay to identify potential shell proteins with low complexity regions which may be missed in the shell proteomic analysis. Indeed, several potential shell proteins including shematrin-like and extremely acidic proteins were identified from the two bivalves, with the former belonging to the tyrosine oxidation-related proteins. Interestingly, further protein database screening revealed the prevalence of shematrin-like proteins in bivalves, gastropods and chitons, and coincided with the presence of CaCO3 exoskeletons in the corresponding species, indicating that shematrin-like proteins play a vital role in molluscan shell mineralization. Considering the potential interaction of the core elements of biomineralization toolkit, we proposed two shell matrix assembly pathways, namely the chitin-based and the shematrin-based pathways, and their potential roles in guiding shell formation. Our study fulfilled some important gaps of the shell matrix assembly in molluscs and led to a comprehensive model for shell mineralization, which not only provides insight into the exoskeleton development but also set some guidelines for future studies for shell proteins.

ORGANISM(S): Atrina Pectinata Crassostrea Gigas X Crassostrea Angulata

SUBMITTER: Chuang Liu  

PROVIDER: PXD055220 | iProX | Fri Aug 23 00:00:00 BST 2024

REPOSITORIES: iProX