Shell Proteome Plasticity Assists Oyster Larval Biomineralization in Adverse Carbonate Chemistry

Bivalve planktonic development is a critical phase during which larvae must secrete the first calcium carbonate shell, the prodissoconch I (PD I). As PD I formation is in close contact with seawater, this process can be negatively affected by adverse seawater carbonate chemistry. It is hypothesized that bivalves can regulate shell formation under environmental stress through biologically controlled biomineralization involving a complex extracellular shell proteome. However, the plasticity of this regulatory mechanism during PD I development is unknown. We assessed the PD I shell proteome of the Hong Kong oyster (Magallana hongkongensis) in carbonate chemistry that was adverse or favorable for biomineralization to understand the regulatory capacity of larval shell formation. While survival rates were not affected in adverse carbonate chemistry, there were significant changes, including the upregulation of several calcium-binding proteins and downregulation of proton-generating processes and putative calcification inhibitors. With 198 sequences, the oyster larval shell proteome was twice to over six times larger than those reported for other bivalve species at the same developmental stage. However, in adverse carbonate chemistry, the oyster larval shells were thinner and smaller, and protein diversity decreased to 131 sequences, with overall lower functional redundancy and reduced expression of structural proteins, indicating potential trade-offs. The proteomic and shell structural data also suggest that direct cellular control and biologically induced mechanisms, which will require further investigation, may be involved in PD I formation.