Exoskeleton protein repertoires in decapod crustaceans revealed distinct biomineralization evolution with molluscs.

ABSTRACT

Crustaceans are the champions of mineral mobilization and deposition in the animal kingdom due to their unique ability to rapidly and periodically mineralize and demineralize their exoskeletons. They are commonly covered with mineralized exoskeletons for protection and regularly molt throughout their lives. Mineralized crustacean exoskeletons are formed under the control of macromolecules especially matrix proteins but the types of matrix proteins are understudied compared to those in molluscan shells. This gap hinders our understanding of their evolutionary paths compared with those of molluscs. Here, we comprehensively analyzed matrix proteins in the exoskeleton of two crabs, one shrimp, and one crayfish and resulted in a major improvement (∼10-fold) in the identification of biomineralization proteins compared to conventional methods for decapod crustaceans. By a comparison with well-studied molluscan biomineralization proteins, we found that decapod crustaceans evolved novel proteins to form mineralized exoskeletons while sharing some proteins with those of molluscs. Our study sheds light on their evolution and adaption to different environment for exoskeleton formation and provides a foundation for further studies of mineralization in crustaceans under normal and climate-changed conditions. SIGNIFICANCE: Most crustaceans have mineralized exoskeletons as protection. How they form these hierarchical structures is still unclear. This is due partially to the understudied matrix proteins in the minerals. This study filled such a gap by using proteomic analysis of matrix proteins from four decapod crustacean exoskeletons. Many novel proteins were discovered which enabled a solid comparison with those of molluscs. By comparison, we proposed that crustaceans evolved novel proteins to form mineralized exoskeletons while sharing some proteins with those of molluscs. This is useful for us to understand the evolution of two major biomineralized phylum.