Biomineralization mechanisms in the estuarine oyster (Crassostrea ariakensis): Unveiling the adaptive potential of mollusks in response to rapid climate change

Abstract

Rapid climate change is often considered detrimental to biomineralization in mollusks; however, accumulating contradictory evidence necessitates reevaluation of the concept. Estuaries, characterized by fluctuating pH levels and limited calcifying substrate availability, are generally considered unfavorable for biomineralization. Understanding how biomineralization evolves in estuarine environments is essential for assessing adaptive potential and identifying mechanisms that could support molluscan adaptation to future environmental change. Phenotypic analyses, multi-omics approaches, and functional assays were employed within a common garden design to investigate the mechanisms underlying the estuarine oyster (Crassostrea ariakensis) adaptation to estuarine environments, using Pacific oysters (Crassostrea gigas), which inhabit non-estuarine areas, as a control. Compared with C. gigas, C. ariakensis exhibited superior biomineralization capacity, evidenced by heavier shells with increased density, enhanced resistance to dissolution, and greater toughness. Ion homeostasis and high expression of classical-pathway mantle secretomes were identified as compensatory mechanisms for the biomineralization adaptation of C. ariakensis. The novel C. ariakensis C-type lectin, a species-specific classical-pathway shell matrix secreted protein (SMSP), demonstrated a high capacity to accelerate the CaCO₃ precipitation rate of calcite particles, thereby underscoring the essential roles of species-specific SMSPs in estuarine adaptations. This study provides novel insights into the adaptive potential of biomineralization in mollusks under rapid climate change. Analyzing biomineralization in estuarine organisms is critical for anticipating the emergent impacts of climate change.