Multi-omic insights into the formation and evolution of a novel shell microstructure in oysters

BMC Biology

Research Article

Yiming Hu¹  Lingfeng Kong¹  Chengxun Xu¹  Hong Yu¹  Shikai Liu¹  Yitian Bai¹  Qi Li² 

[1] Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, 266003, Qingdao, China;Key Laboratory of Mariculture, Ministry of Education, Ocean University of China, 266003, Qingdao, China;Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, 266237, Qingdao, China;

关键词: Biomineralization;    Oyster;    Shell;    Chalky layer;    Genome;    Pif evolution;    Neo-functionalization;   

DOI  :  10.1186/s12915-023-01706-y

 received in 2023-06-01, accepted in 2023-09-18,  发布年份 2023

来源: Springer

【 摘 要 】

BackgroundMolluscan shell, composed of a diverse range of architectures and microstructures, is a classic model system to study the relationships between molecular evolution and biomineralized structure formation. The shells of oysters differ from those of other molluscs by possessing a novel microstructure, chalky calcite, which facilitates adaptation to the sessile lifestyle. However, the genetic basis and evolutionary origin of this adaptive innovation remain largely unexplored.ResultsWe report the first whole-genome assembly and shell proteomes of the Iwagaki oyster Crassostrea nippona. Multi-omic integrative analyses revealed that independently expanded and co-opted tyrosinase, peroxidase, TIMP genes may contribute to the chalky layer formation in oysters. Comparisons with other molluscan shell proteomes imply that von Willebrand factor type A and chitin-binding domains are basic members of molluscan biomineralization toolkit. Genome-wide identification and analyses of these two domains in 19 metazoans enabled us to propose that the well-known Pif may share a common origin in the last common ancestor of Bilateria. Furthermore, Pif and LamG3 genes acquire new genetic function for shell mineralization in bivalves and the chalky calcite formation in oysters likely through a combination of gene duplication and domain reorganization.ConclusionsThe spatial expression of SMP genes in the mantle and molecular evolution of Pif are potentially involved in regulation of the chalky calcite deposition, thereby shaping the high plasticity of the oyster shell to adapt to a sessile lifestyle. This study further highlights neo-functionalization as a crucial mechanism for the diversification of shell mineralization and microstructures in molluscs, which may be applied more widely for studies on the evolution of metazoan biomineralization.

【 授权许可】

CC BY   
© BioMed Central Ltd., part of Springer Nature 2023

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