Temporal proteomic profiling reveals insight into critical developmental processes and temperature-influenced physiological response differences in a bivalve mollusc

Protein expression patterns underlie physiological processes and phenotypic differences including those occurring during early development. The Pacific oyster (Crassostrea gigas) is particularly fascinating as it undergoes a dramatic transformation from free-swimming larval form to sessile benthic dweller, and proliferates in environments widely ranging in temperature. Here, we comprehensively characterized protein expression patterns for 7978 proteins throughout metamorphosis in the Pacific oyster at two temperature regimes to gain a better understanding of how developmental processes are altered. We used a multi-statistical approach including principal component analysis, ANOVA-simultaneous component analysis, and hierarchical clustering coupled with functional enrichment analysis to characterize these data. We identified distinct sets of proteins with time-dependent abundances generally not affected by temperature. Over time, adhesion and calcification related proteins acutely decreased, organogenesis and extracellular matrix related proteins gradually decreased, proteins related to signalling showed sinusoidal abundance patterns, and proteins related to metabolic and growth processes gradually increased. Contrastingly, different sets of proteins showed temperature-dependent abundance patterns with proteins related to immune response showing lower abundance and catabolic pro-growth processes showing higher abundance in animals reared at 29°C relative to 23°C. These abundance pattern differences correspond to larger oyster size observed at the elevated temperature and are likely indicative of a combination of differences in specific metamorphic processes and possible pathogen presence. The proteome resource generated by this study provides data-driven guidance for future work on developmental changes in molluscs. Furthermore, the analytical approach taken here provides a foundation for effective shotgun proteomic analyses across a variety of taxa.