title: Nanoconfined β-sheets mechanically reinforce the supra-biomolecular network of robust squid Sucker Ring Teeth.
abstract: 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.
authors.forename: Paul A
authors.initials: PA
authors.lastname: Guerette
authors.forename: Shawn
authors.initials: S
authors.lastname: Hoon
authors.forename: Dawei
authors.initials: D
authors.lastname: Ding
authors.forename: Shahrouz
authors.initials: S
authors.lastname: Amini
authors.forename: Admir
authors.initials: A
authors.lastname: Masic
authors.forename: Vydianathan
authors.initials: V
authors.lastname: Ravi
authors.forename: Byrappa
authors.initials: B
authors.lastname: Venkatesh
authors.forename: James C
authors.initials: JC
authors.lastname: Weaver
authors.forename: Ali
authors.initials: A
authors.lastname: Miserez
mesh_terms: D000595:Amino Acid Sequence; D000818:Animals; D001696:Biomechanical Phenomena; D040761:Biomimetic Materials / Q000737:chemistry; D049832:Decapodiformes / Q000033:anatomy & histology / Q000235:genetics; D029941:Fish Proteins / Q000737:chemistry / Q000235:genetics; D006860:Hydrogen Bonding; D055595:Mechanical Phenomena; D008958:Models, Molecular; D008969:Molecular Sequence Data; D049329:Nanostructures / Q000737:chemistry*; D055550:Protein Stability; D017433:Protein Structure, Secondary; D059467:Transcriptome
chemical_list: D029941:Fish Proteins