Paul A. Guerette1,2,*, Shawn Hoon3,4,*, Dawei Ding1, Shahrouz Amini1, Admir Masic5, Vydianathan Ravi6, Byrappa Venkatesh6, James C. Weaver7, and Ali Miserez1,4
1 School of Materials Science and Engineering, Nanyang Technological University, 50 Nanyang Avenue, Singapore 639798
2 Energy Research Institute at Nanyang Technological University (ERI@N), 50 Nanyang Drive, Singapore 637553
3 Molecular Engineering Lab, Biomedical Sciences Institutes, A*STAR, 61 Biopolis Drive, Proteos, Singapore 138673
4 School of Biological Sciences, Nanyang Technological University, 60 Nanyang Drive, Singapore 637551
5 Department of Biomaterials, Max-Planck Institute of Colloids and Interfaces, Research Campus Golm, 14424 Potsdam, Germany
6 Institute of Molecular and Cell Biology, A*STAR, 61 Biopolis Drive, Proteos, Singapore 138673
7 Wyss Institute for Biologically Inspired Engineering, Harvard University, 60 Oxford Street, Cambridge, Massachusetts 02138, United States
*contributed equally to this work.
Published online in ACS Nano on 6 June 2014.
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The predatory efficiency of squid and cuttlefish (superorder Decapodiformes) is enhanced by robust Sucker Ring Teeth (SRT) that perform grappling functions during prey capture. Here, we show that SRT are composed entirely of related structural “suckerin” proteins whose modular designs enable the formation of nanoconfined β-sheet-reinforced polymer networks. Thirty-seven previously undiscovered suckerins were identified from transcriptomes assembled from three distantly related decapodiform cephalopods. Similarity in modular sequence design and exon–intron architecture suggests that suckerins are encoded by a multigene family. Phylogenetic analysis supports this view, revealing that suckerin genes originated in a common ancestor 350 MYa and indicating that nanoconfined β-sheet reinforcement is an ancient strategy to create robust bulk biomaterials. X-ray diffraction, nanomechanical, and micro-Raman spectroscopy measurements confirm that the modular design of the suckerins facilitates the formation of β-sheets of precise nanoscale dimensions and enables their assembly into structurally robust supramolecular networks stabilized by cooperative hydrogen bonding. The suckerin gene family has likely played a key role in the evolutionary success of decapodiform cephalopods and provides a large molecular toolbox for biomimetic materials engineering.
Figure Legend: Morphology and composition of sucker ring teeth (SRT) from three distantly related cephalopods. (A) Scalar relationships of D. gigas (top), S. lessoniana (middle), and S. esculenta (bottom) and their respective SRT (B). (C) Large-scale modular architecture of suckerin proteins from D. gigas (left), S. lessoniana (right-top), and S. esculenta (right-bottom).
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