Transcriptome-To-Phenome Response of Larval Eastern Oysters Under Multiple Drivers of Aragonite Undersaturation

Understanding how interactive environmental challenges affect marine species is critical to long-term ecological and economic stability under global change. Marine calcifiers are thought to be vulnerable to ocean acidification (OA; elevated pCO₂); active dissolution of aragonite (Ωar) is associated with disrupted development, survivorship, and gene expression in bivalve larvae, resulting in an early life-stage bottleneck. Dynamic carbonate chemistry in coastal systems emphasizes the importance of multiple stressors, e.g., warming and low salinity events may change organismal responses relative to OA alone. We exposed Eastern oyster larvae (Crassostrea virginica) to a full-factorial experimental design using two temperatures (23°C and 27°C), salinities (17 and 27), and pCO₂ levels (~700 μatm and 1850 μatm pCO₂), resulting in Ωar conditions 0.3-1.7. Ωar reduced by low salinity, elevated pCO₂, and low temperature, each slowed early development and reduced survival. Low salinity × elevated pCO₂ was linked to severe Ωar undersaturation (< 0.5) that suppressed expression of bicarbonate transport, biomineralization and augmented expression for ciliary locomotion, proteostasis, and histone modifiers. In isolation and under moderate Ωar intensity (0.5 < Ωar < 1), larvae increased transcription for osmoregulatory activity and endocytosis under low salinity, and suppressed transcription for iron metabolism under elevated pCO₂. Although shell growth and survival were affected by Ωar undersaturation, gene expression patterns of D-stage oyster larvae and oyster juveniles suggests tolerance to dynamic estuarine environments. Genes and expression patterns that confer survival of postmetamorphosed oysters can improve our understanding of environmental-organismal interactions and improve breeding programs enabling sustainable production.