In-depth proteomic analysis of shell matrix proteins of Pinctada fucata

Abstract

The shells of pearl oysters, Pinctada fucata, are composed of calcite and aragonite and possess remarkable mechanical properties. These shells are formed under the regulation of macromolecules, especially shell matrix proteins (SMPs). Identification of diverse SMPs will lay a foundation for understanding biomineralization process. Here, we identified 72 unique SMPs using liquid chromatography-tandem mass spectrometry (LC-MS/MS) analysis of proteins extracted from the shells of P. fucata combined with a draft genome. Of 72 SMPs, 17 SMPs are related to both the prismatic and nacreous layers. Moreover, according to the diverse domains found in the SMPs, we hypothesize that in addition to controlling CaCO3 crystallization and crystal organization, these proteins may potentially regulate the extracellular microenvironment and communicate between cells and the extracellular matrix (ECM). Immunohistological localization techniques identify the SMPs in the mantle, shells and synthetic calcite. Together, these proteomic data increase the repertoires of the shell matrix proteins in P. fucata and suggest that shell formation in P. fucata may involve tight regulation of cellular activities and the extracellular microenvironment.

Identification of conserved proteins from diverse shell matrix proteome in Crassostrea gigas: characterization of genetic bases regulating shell formation

“…In C. gigas SMPEs, 66 out of the SMPE-Cg3 and 47 out of the SMPE-Cg2 were predicted to have at least one region of ID (Supplementary Table S1). This is higher than that found in P. fucata which contained 22 ID proteins out of the 35 SMPs10. XSTREAM analysis predicted that 24 out of SMPE-Cg3 and 21 out of SMPE-Cg2 proteins to contain tandem repeats in C. gigas, which is higher than that reported in P. fucata ( 7 out of 35).…”

“…The mantle is divided into distinct morphogenetic regions consisting of highly specialized epithelial cell types9. The mantle produces shell matrix proteins (SMPs) that play important roles in crystal nucleation, polymorphism, morphology, and organization of CaCO 3 crystallites during shell formation10.…”

“…Recently, high-throughput transcriptomics and proteomics analyses have been successively used to characterize shell matrix proteomes (SMPEs) in Haliotis asinina 8, Pinctada margaritifera 12, Pinctada maxima 12, Crassostrea gigas 13, Lottia gigantea 14, Cepaea nemoralis 6, Mytilus coruscus 15, Pinctada. fucata 10, Magellania venosa 2, Mytilus galloprovincialis 16, Mya truncata 17, and C. gigas, Mytilus edulis , and Pecten maximus 18. However, only two global SMPEs comparisons have been performed in C. nemoralis and M. venosa , revealing low similarities.…”

“…Even in bivalves, two different models have been proposed for calcifying shell formation. The well-known matrix model of “chitin-silk fibroin gel proteins-acidic macromolecules” largely explained biomineralization in P. fucata from a crystal growth perspective1019. While the cellular model shows that shell formation is orchestrated by cells and the extracellular matrix (ECM) and crystals are formed in haemocytes in eastern oyster, Crassostrea virginica 2021.…”

Deep conservation of bivalve nacre proteins highlighted by shell matrix proteomics of the Unionoida Elliptio complanata and Villosa lienosa

“…Recently, this enzyme has also been detected in lesser amounts in nacre rsif.royalsocietypublishing.org J. R. Soc. Interface 14: 20160846 shell structure [16]. Tyrosinase is an oxidase that controls the production of protein melanogenesis via cross-linking by hydroxylation of the phenol groups present in tyrosine residues and their conversion to quinones.…”