Insights from the Shell Proteome: Biomineralization to Adaptation

Abstract

Bivalves have evolved a range of complex shell forming mechanisms that are reflected by their incredible diversity in shell mineralogy and microstructures. A suite of proteins exported to the shell matrix space plays a significant role in controlling these features, in addition to underpinning some of the physical properties of the shell itself. Although, there is a general consensus that a minimum basic protein tool kit is required for shell construction, to date, this remains undefined. In this study, the shell matrix proteins (SMPs) of four highly divergent bivalves (The Pacific oyster, Crassostrea gigas; the blue mussel, Mytilus edulis; the clam, Mya truncata, and the king scallop, Pecten maximus) were analyzed in an identical fashion using proteomics pipeline. This enabled us to identify the critical elements of a "basic tool kit" for calcification processes, which were conserved across the taxa irrespective of the shell morphology and arrangement of the crystal surfaces. In addition, protein domains controlling the crystal layers specific to aragonite and calcite were also identified. Intriguingly, a significant number of the identified SMPs contained domains related to immune functions. These were often are unique to each species implying their involvement not only in immunity, but also environmental adaptation. This suggests that the SMPs are selectively exported in a complex mix to endow the shell with both mechanical protection and biochemical defense.

Keywords: aragonite; biomineralization; calcification; calcite; evolution; shell matrix proteins.

Fig. 1

Phylogeny of four bivalve models and their corresponding divergence times based on a Bayesian analysis using mitochondrial genes (Plazzi and Passamonti 2010; Ren et al. 2010).

Fig. 2

Circos representation of the sequence similarities of identified SMPs from the four bivalve models (cut-off E-value ≥ e⁻¹⁰). Colored lines represent similarity scores, with the corresponding E-values denoted in the figure.

Fig. 3

Venn diagram of the protein-domains identified from the four bivalve SMPs. Domains common to the four bivalve models are indicated in white. Domains in yellow and green are related to calcite and aragonite shell layers. Immunity-related domains are represented in red.

Fig. 4

Representation of the phenoloxidase oxidation pathway in arthropods adapted from Jiravanichpaisal et al. (2006). The boxed annotations show the identified functional domains and their corresponding protein families in this activation pathway.