Nacre, the iridescent material found in pearls and shells of molluscs, is formed through an extraordinary process of matrix-assisted biomineralization. Despite recent advances, many aspects of the biomineralization process and its evolutionary origin remain unknown. The pearl oyster Pinctada fucata martensii is a well-known master of biomineralization, but the molecular mechanisms that underlie its production of shells and pearls are not fully understood. We sequenced the highly polymorphic genome of the pearl oyster and conducted multi-omic and biochemical studies to probe nacre formation. We identified a large set of novel proteins participating in matrix-framework formation, many in expanded families, including components similar to that found in vertebrate bones such as collagen-related VWA-containing proteins, chondroitin sulfotransferases, and regulatory elements. Considering that there are only collagen-based matrices in vertebrate bones and chitin-based matrices in most invertebrate skeletons, the presence of both chitin and elements of collagen-based matrices in nacre suggests that elements of chitin- and collagen-based matrices have deep roots and might be part of an ancient biomineralizing matrix. Our results expand the current shell matrix-framework model and provide new insights into the evolution of diverse biomineralization systems.

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Pearl oysters are found in the marine ecosystem. Due to their frequent exposure to microbial pathogens and environmental perturbations, they have developed a multifaceted innate immune system with differentially expressed immune‐related genes in response to a range of stress via vast coordinated immune reactions, such as immune recognition, signal transduction, synthesis of antimicrobial peptides, encapsulation and phagocytosis of the circulating haemocytes. The species are farmed to produce pearls. With the increasing adoption of aquaculture techniques in pearl production, there is the need to understand their culture environment and their immune response mechanisms. Multi‐omic studies have documented responses to nuclei insertion operation, diseases and various environmental conditions in Pinctada fucata martensii (Dunker, 1880), Pinctada maxima (Jameson, 1901), Pinctada margaritifera and Pteria penguin (Roding, 1798). Among the various stressors, nuclei insertion operation has been identified as a prevailing factor modifying gene expression. Other factors include life stage, air exposure, temperature, salinity, metals and organic contaminants. This manuscript details the response mechanism of these pearl oysters to the various stressors.