A diecast mineralization process forms the tough mantis shrimp dactyl club
Biomineralization, the process by which mineralized tissues grow and harden via biogenic mineral deposition, is a relatively lengthy process in many mineral-producing organisms, resulting in challenges to study the growth and biomineralization of complex hard mineralized tissues. Arthropods are idea...
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sg-ntu-dr.10356-1514232021-09-23T02:21:12Z A diecast mineralization process forms the tough mantis shrimp dactyl club Amini, Shahrouz Tadayon, Maryam Loke, Jun Jie Kumar, Akshita Kanagavel, Deepankumar Le Ferrand, Hortense Duchamp, Martial Raida, Manfred Sobota, Radoslaw M. Chen, Liyan Hoon, Shawn Miserez, Ali School of Biological Sciences School of Materials Science and Engineering Centre for Biomimetic Sensor Science (CBSS) Science::Biological sciences Biomineralization Bioapatite Biomineralization, the process by which mineralized tissues grow and harden via biogenic mineral deposition, is a relatively lengthy process in many mineral-producing organisms, resulting in challenges to study the growth and biomineralization of complex hard mineralized tissues. Arthropods are ideal model organisms to study biomineralization because they regularly molt their exoskeletons and grow new ones in a relatively fast timescale, providing opportunities to track mineralization of entire tissues. Here, we monitored the biomineralization of the mantis shrimp dactyl club—a model bioapatite-based mineralized structure with exceptional mechanical properties—immediately after ecdysis until the formation of the fully functional club and unveil an unusual development mechanism. A flexible membrane initially folded within the club cavity expands to form the new club’s envelope. Mineralization proceeds inwards by mineral deposition from this membrane, which contains proteins regulating mineralization. Building a transcriptome of the club tissue and probing it with proteomic data, we identified and sequenced Club Mineralization Protein 1 (CMP-1), an abundant mildly phosphorylated protein from the flexible membrane suggested to be involved in calcium phosphate mineralization of the club, as indicated by in vitro studies using recombinant CMP-1. This work provides a comprehensive picture of the development of a complex hard tissue, from the secretion of its organic macromolecular template to the formation of the fully functional club. Agency for Science, Technology and Research (A*STAR) National Research Foundation (NRF) This work was funded by the Singapore National Research Foundation (NRF) through an individual NRF Fellowship (to A.M.), and by the Strategic Initiative on Biomimetic and Sustainable Materials (IBSM, NTU). H.L.F. gratefully acknowledges the Swiss National Science Foundation for an individual postdoctoral scholarship (Grant_P2EZP2_172169). R.M.S. and L.C. were supported by A*Star core funding. 2021-09-23T02:21:11Z 2021-09-23T02:21:11Z 2019 Journal Article Amini, S., Tadayon, M., Loke, J. J., Kumar, A., Kanagavel, D., Le Ferrand, H., Duchamp, M., Raida, M., Sobota, R. M., Chen, L., Hoon, S. & Miserez, A. (2019). A diecast mineralization process forms the tough mantis shrimp dactyl club. Proceedings of the National Academy of Sciences of the United States of America, 116(18), 8685-8692. https://dx.doi.org/10.1073/pnas.1816835116 0027-8424 https://hdl.handle.net/10356/151423 10.1073/pnas.1816835116 30975751 2-s2.0-85065511215 18 116 8685 8692 en Proceedings of the National Academy of Sciences of the United States of America © 2019 The Author(s). Published by National Academy of Sciences. All rights reserved. |
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Science::Biological sciences Biomineralization Bioapatite Amini, Shahrouz Tadayon, Maryam Loke, Jun Jie Kumar, Akshita Kanagavel, Deepankumar Le Ferrand, Hortense Duchamp, Martial Raida, Manfred Sobota, Radoslaw M. Chen, Liyan Hoon, Shawn Miserez, Ali A diecast mineralization process forms the tough mantis shrimp dactyl club |
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Biomineralization, the process by which mineralized tissues grow and harden via biogenic mineral deposition, is a relatively lengthy process in many mineral-producing organisms, resulting in challenges to study the growth and biomineralization of complex hard mineralized tissues. Arthropods are ideal model organisms to study biomineralization because they regularly molt their exoskeletons and grow new ones in a relatively fast timescale, providing opportunities to track mineralization of entire tissues. Here, we monitored the biomineralization of the mantis shrimp dactyl club—a model bioapatite-based mineralized structure with exceptional mechanical properties—immediately after ecdysis until the formation of the fully functional club and unveil an unusual development mechanism. A flexible membrane initially folded within the club cavity expands to form the new club’s envelope. Mineralization proceeds inwards by mineral deposition from this membrane, which contains proteins regulating mineralization. Building a transcriptome of the club tissue and probing it with proteomic data, we identified and sequenced Club Mineralization Protein 1 (CMP-1), an abundant mildly phosphorylated protein from the flexible membrane suggested to be involved in calcium phosphate mineralization of the club, as indicated by in vitro studies using recombinant CMP-1. This work provides a comprehensive picture of the development of a complex hard tissue, from the secretion of its organic macromolecular template to the formation of the fully functional club. |
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School of Biological Sciences |
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School of Biological Sciences Amini, Shahrouz Tadayon, Maryam Loke, Jun Jie Kumar, Akshita Kanagavel, Deepankumar Le Ferrand, Hortense Duchamp, Martial Raida, Manfred Sobota, Radoslaw M. Chen, Liyan Hoon, Shawn Miserez, Ali |
format |
Article |
author |
Amini, Shahrouz Tadayon, Maryam Loke, Jun Jie Kumar, Akshita Kanagavel, Deepankumar Le Ferrand, Hortense Duchamp, Martial Raida, Manfred Sobota, Radoslaw M. Chen, Liyan Hoon, Shawn Miserez, Ali |
author_sort |
Amini, Shahrouz |
title |
A diecast mineralization process forms the tough mantis shrimp dactyl club |
title_short |
A diecast mineralization process forms the tough mantis shrimp dactyl club |
title_full |
A diecast mineralization process forms the tough mantis shrimp dactyl club |
title_fullStr |
A diecast mineralization process forms the tough mantis shrimp dactyl club |
title_full_unstemmed |
A diecast mineralization process forms the tough mantis shrimp dactyl club |
title_sort |
diecast mineralization process forms the tough mantis shrimp dactyl club |
publishDate |
2021 |
url |
https://hdl.handle.net/10356/151423 |
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1712300624193781760 |