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A Diecast Mineralization Process Forms the Tough Mantis Shrimp Dactyl Club

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A Diecast Mineralization Process Forms the Tough Mantis Shrimp Dactyl Club A diecast mineralization process forms the tough mantis shrimp dactyl club Shahrouz Aminia, Maryam Tadayona, Jun Jie Lokea, Akshita Kumara, Deepankumar Kanagavela, Hortense Le Ferranda, Martial Duchampb, Manfred Raidac, Radoslaw M. Sobotad, Liyan Chend, Shawn Hoone, and Ali Misereza,f,1 aCentre for Biomimetic Sensor Science, School of Materials Science and Engineering, Nanyang Technological University (NTU), 639798 Singapore; bSchool of Materials Science and Engineering, NTU, 639798 Singapore; cLife Science Institutes, Singapore Lipidomics Incubator, National University of Singapore (NUS), 117456 Singapore; dFunctional Proteomics Laboratory, Institute for Molecular, Cell, and Development Biology, Agency for Science, Technology, and Research (A*Star), 138673 Proteos, Singapore; eMolecular Engineering Laboratory, Biomedical Sciences Institutes, A*Star, 138673 Proteos, Singapore; and fSchool of Biological Sciences, NTU, 637551 Singapore Edited by Lia Addadi, Weizmann Institute of Science, Rehovot, Israel, and approved March 19, 2019 (received for review October 2, 2018) Biomineralization, the process by which mineralized tissues grow We used the dactyl club of stomatopods (mantis shrimps) as a and harden via biogenic mineral deposition, is a relatively lengthy model structure to study the entire formation of hard and tough process in many mineral-producing organisms, resulting in challenges apatite-based mineralized appendages. The club is a biological to study the growth and biomineralization of complex hard miner- hammer used by stomatopods to fracture the hard shells of their alized tissues. Arthropods are ideal model organisms to study preys and has emerged in recent years as a fascinating model biomineralization because they regularly molt their exoskeletons structure of bioinspired materials (6–10). The club is the most and grow new ones in a relatively fast timescale, providing oppor- mineralized appendage of the dactyl segment and exhibits a tunities to track mineralization of entire tissues. Here, we monitored complex architecture across multiple length scales, allowing the the biomineralization of the mantis shrimp dactyl club—amodel animal to deliver extremely high impact forces against its targets bioapatite-based mineralized structure with exceptional mechanical without sustaining macroscopic fracture. In brief, the dactyl club — properties immediately after ecdysis until the formation of the fully is a multilayer composite at the mesoscale that can be broadly functional club and unveil an unusual development mechanism. A separated into an outer region that expands toward the impact flexible membrane initially folded within the club cavity expands to surface and an inner bulk region. Both regions exhibit distinct BIOPHYSICS AND form the new club’s envelope. Mineralization proceeds inwards by chemical compositions and microstructures. The outer region is COMPUTATIONAL BIOLOGY mineral deposition from this membrane, which contains proteins reg- mostly made of crystalline fluorapatite (FAP) nanorods that are ulating mineralization. Building a transcriptome of the club tissue and preferentially oriented perpendicular to the impact surface, with probing it with proteomic data, we identified and sequenced Club a small presence of calcium sulfate (7). Moving toward the bulk, Mineralization Protein 1 (CMP-1), an abundant mildly phosphorylated crystallinity of FAP decreases and the mineral phase gradually protein from the flexible membrane suggested to be involved in cal- cium phosphate mineralization of the club, as indicated by in vitro transitions toward amorphous calcium phosphate (ACP). The inner bulk region contains both ACP as well as amorphous cal- studies using recombinant CMP-1. This work provides a comprehen- BIOCHEMISTRY sive picture of the development of a complex hard tissue, from the cium carbonate (ACC) that decorate chitin fibrils arranged in a secretion of its organic macromolecular template to the formation of the fully functional club. Significance biomineralization | bioapatite | ecdysis | stomatopod dactyl club | Monitoring hard tissues calcification using vertebrates is chal- mineralization proteins lenging, owing to the internal location and slow biomineraliza- tion process of these tissues. Crustaceans are ideal model ard mineralized tissues grow through biogenic mineral de- organisms to overcome this challenge because they regularly Hposition (biomineralization) and this process is a central molt their exoskeletons. Using the ultratough mantis shrimp attribute of vertebrate development (1). However, investigating dactyl club as a model biomineral, we detect all stages during the growth process of entire hard tissues in vertebrates such as the development of a calcified tissue, from secretion of the bone or teeth is challenging, owing to the relatively long timescale organic template that regulates mineral deposition to matu- ration of the functional club. We unveil a peculiar growth over which mineralized tissues are formed (2, 3) and to sample mechanism: a flexible membrane initially folded in the club availability. In contrast, crustaceans are convenient model organ- cavity expands after ecdysis to form the new club outer en- isms to study biomineralization because they regularly shed their velope from which biomineralization proceeds. A main phos- mineralized exoskeletons (cuticles) and grow new ones through phorylated protein within that membrane is sequenced and molting cycles (4, 5). Specifically, molting and calcification of cu- demonstrated to regulate mineral crystal growth. ticles occur in just a few days or weeks, providing the distinctive opportunity to follow the entire biomineralization process for Author contributions: S.A. and A.M. designed research; S.A., M.T., J.J.L., A.K., D.K., H.L.F., model organisms that can be maintained in the laboratory. M.R., R.M.S., L.C., and S.H. performed research; S.A., J.J.L., A.K., H.L.F., M.D., M.R., R.M.S., Molting, the shedding (or ecdysis) of the exoskeleton, is an L.C., S.H., and A.M. analyzed data; and S.A. and A.M. wrote the paper. essential event of arthropod development, during which the hard The authors declare no conflict of interest. exoskeleton is replaced with a fresher, slightly larger one to ac- This article is a PNAS Direct Submission. commodate the animal’s growth. Following molting, the freshly Published under the PNAS license. formed exoskeleton is still soft and cannot fulfill its function, Data deposition: Transriptomic data of O. scyllarus dactyl club have been deposited in the NCBI BioProject (accession no. PRJNA528158. Proteomic data have been deposited in namely providing a protecting barrier against predators, pathogens, the jPOST Repository, https://repository.jpostdb.org (accession no. JPST000563), and in the or the natural environment. Whereas molting takes just a few mi- ProteomeXchange Consortium database (accession no. PXD013153). nutes, mineralization of the new exoskeleton is longer, from days to 1To whom correspondence should be addressed. Email: [email protected]. weeks. Nevertheless, compared with vertebrate mineralization, the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. process is short enough such that the different stages can be studied 1073/pnas.1816835116/-/DCSupplemental. in the laboratory with convenient model organisms (5). www.pnas.org/cgi/doi/10.1073/pnas.1816835116 PNAS Latest Articles | 1of8 Downloaded by guest on October 2, 2021 helicoidal pattern (6, 10). Collectively this multilayer design en- club, mostly composed of organic phases, as shown by the high dows the club with exceptional tolerance against contact stresses carbon content and the absence of calcium. We also note the pres- (8) and serves as inspiration for the design of damage-tolerant ence of sulfur in the premolt membrane, which may act as a reservoir biocomposites (11, 12). for calcium sulfate that is also found in the fully formed clubs (7). The fresh cuticle does not provide protection against external Molting Stages of the Mantis Shrimp threats: although the expanded membranes displayed the overall Mantis shrimps shed their exoskeletons a few times per year. During geometry of a mature club, they were not functional due to their this process, they are vulnerable to attacks from other predators weak mechanical properties (they could easily be bent and torn by (such as crabs, their congeners, or starfish) since their raptorial hand), which explains why mantis shrimps refuse to hit any target appendages are not functional for either hunting or defense pur- and hid inside their nest after ecdysis. Since their survival depends poses. To mitigate this drawback, in the premolt stage, mantis on a fully functional dactyl club, they must rapidly build a new one, shrimps secure a nest by shattering rocks, shells, and corals and then thus providing a unique opportunity to study the entire bio- collect the broken pieces to build a protecting nesting cavity (SI mineralization process. In our aquaria containing artificial seawater, Appendix,Fig.S1A–C). During this process, the dactyl clubs are we found that a partially functional club was formed within a week. eroded on their impact surface due to high-energy hits against rock- solid targets (SI Appendix,Fig.S1E and F), though they do no Formation of the Club by a Diecast Mechanism sustain catastrophic fracture. Subsequently during the molting pe- We followed our initial observations of the molting process with riod, stomatopods hide in this
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