Calcium carbonate polymorph selection in fish otoliths: A key role of phosphorylation of Starmaker-like protein

ACTA BIOMATERIALIA(2024)

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摘要
Fish otoliths are calcium carbonate biominerals found in the inner ear commonly used for tracking fish biochronologies and as a model system for biomineralization. The process of fish otolith formation is bio-logically controlled by numerous biomacromolecules which not only affect crystal size, shape, mechanical properties, but also selection of calcium carbonate polymorph (e.g., aragonite, vaterite). The proteinaceous control over calcium carbonate polymorph selection occurs in many other species (e.g., corals, mollusks, echinoderms) but the exact mechanism of protein interactions with calcium and carbonate ions - con-stituents of CaCO3 - are not fully elucidated. Herein, we focus on a native Starmaker-like protein iso-lated from vaterite asteriscus otoliths from Cyprinus carpio. The proteomic studies show the presence of the phosphorylated protein in vaterite otoliths. In a series of in vitro mineralization experiments with Starmaker-like, we show that native phosphorylation is a crucial determinant for the selection of a crys-tal's polymorphic form. This is the first report showing that the switch in calcium carbonate phase de -pends on the phosphorylation pattern of a single isolated protein. Statement of Significance Calcium carbonate has numerous applications in industry and medicine. However, we still do not un-derstand the mechanism of biologically driven polymorph selection which results in specific biomineral properties. Previous work on calcium carbonate biominerals showed that either several macromolecular factors or high magnesium concentration (non-physiological) are required for proper polymorph selec-tion (e.g., in mollusk shells, corals and otoliths). In this work, we showed for the first time that protein phosphorylation is a crucial factor for controlling the calcium carbonate crystal phase. This is important because a single protein from the otolith organic matrix could switch between polymorphs depending on the phosphorylation level. It seems that protein post-translational modifications (native, not artificial) are more important for biomolecular control of crystal growth than previously considered. (c) 2023 The Authors. Published by Elsevier Ltd on behalf of Acta Materialia Inc. This is an open access article under the CC BY-NC-ND license ( http://creativecommons.org/licenses/by-nc-nd/4.0/ )
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关键词
Biomineralization,Intrinsically disordered protein,Organic matrix,Post-translational modifications,Vaterite asteriscus,Mineral phase
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