Biomineralization is a widespread metazoan process involving controlled inorganic mineral deposition within organic matrices, mediated by organic-inorganic interactions. The rapid evolution of biomineralized shells during the Cambrian period significantly contributed to the success of molluscs. While biomineralization in shallow-water molluscs is well-studied, its biomolecular basis in deep-sea lineages, which occupy more recently diverged branches, remains poorly understood. Deciphering these mechanisms can reveal evolutionary innovations in extreme environments, molecular interactions governing biomineralization, and potential applications in bioinspired material design.
This study investigates deep-sea molluscan shell formation through comparative multi-omics (genomics, transcriptomics, and proteomics) and microstructural analyses. We focus on bivalves and gastropods from hydrothermal vents and methane seeps to elucidate mineralization under extreme conditions. Chromosome-level genome assembly of the deep-sea limpet Bathyacmaea lactea enabled gene family studies on adaptive biomineralization. In situ shell repair experiments in the deep-sea mussel Gigantidas haimaensis and its shallow-water relative Modiolus philippinarum revealed enhanced organic matrix production during regeneration in deep-sea species. Additionally, the scaly-foot snail’s unique dual-shell system demonstrated repurposed ancestral biomineralization "tool-kits" for novel hard-part formation. Collectively, our work systematically uncovers adaptive biomineralization mechanisms across deep-sea ecosystems, expanding the known repertoire of mineralization strategies. These findings advance our understanding of evolutionary developmental processes in extreme environments and may inspire pressure-tolerant composite material design.