Mussels are opportunistic macrofouling organisms that can attach to most immersed solid surfaces, leading to serious economic and ecological consequences for the maritime and aquaculture industries. We demonstrate that lubricant-infused coatings exhibit very low preferential mussel attachment and ultralow adhesive strengths under both controlled laboratory conditions and in marine field studies. Detailed investigations across multiple length scales-from the molecular-scale characterization of deposited adhesive proteins to nanoscale contact mechanics to macroscale live observations-suggest that lubricant infusion considerably reduces fouling by deceiving the mechanosensing ability of mussels, deterring secretion of adhesive threads, and decreasing the molecular work of adhesion. Our study demonstrates that lubricant infusion represents an effective strategy to mitigate marine biofouling and provides insights into the physical mechanisms underlying adhesion prevention.
Efforts to engineer new materials inspired by biological structures are hampered by the lack of genomic data from many model organisms studied in biomimetic research. Here we show that biomimetic engineering can be accelerated by integrating high-throughput RNA-seq with proteomics and advanced materials characterization. This approach can be applied to a broad range of systems, as we illustrate by investigating diverse high-performance biological materials involved in embryo protection, adhesion and predation. In one example, we rapidly engineer recombinant squid sucker ring teeth proteins into a range of structural and functional materials, including nanopatterned surfaces and photo-cross-linked films that exceed the mechanical properties of most natural and synthetic polymers. Integrating RNA-seq with proteomics and materials science facilitates the molecular characterization of natural materials and the effective translation of their molecular designs into a wide range of bio-inspired materials.
The bulk of Earth’s biological materials consist of few base substances—essentially proteins, polysaccharides, and minerals—that assemble into large varieties of structures. Multifunctionality arises naturally from this structural complexity: An example is the combination of rigidity and flexibility in protein-based teeth of the squid sucker ring. Other examples are time-delayed actuation in plant seed pods triggered by environmental signals, such as fire and water, and surface nanostructures that combine light manipulation with mechanical protection or water repellency. Bioinspired engineering transfers some of these structural principles into technically more relevant base materials to obtain new, often unexpected combinations of material properties. Less appreciated is the huge potential of using bioinspired structural complexity to avoid unnecessary chemical diversity, enabling easier recycling and, thus, a more sustainable materials economy.
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.
Interfacial water constitutes a formidable barrier to strong surface bonding, hampering the development of water-resistant synthetic adhesives. Notwithstanding this obstacle, the Asian green mussel Perna viridis attaches firmly to underwater surfaces via a proteinaceous secretion (byssus). Extending beyond the currently known design principles of mussel adhesion, here we elucidate the precise time-regulated secretion of P. viridis mussel adhesive proteins. The vanguard 3,4-dihydroxy-L-phenylalanine (Dopa)-rich protein Pvfp-5 acts as an adhesive primer, overcoming repulsive hydration forces by displacing surface-bound water and generating strong surface adhesion. Using homology modelling and molecular dynamics simulations, we find that all mussel adhesive proteins are largely unordered, with Pvfp-5 adopting a disordered structure and elongated conformation whereby all Dopa residues reside on the protein surface. Time-regulated secretion and structural disorder of mussel adhesive proteins appear essential for optimizing extended nonspecific surface interactions and byssus' assembly. Our findings reveal molecular-scale principles to help the development of wet-resistant adhesives.
Stomatopods are shallow-water crustaceans that employ powerful dactyl appendages to hunt their prey. Deployed at high velocities, these hammer-like clubs or spear-like devices are able to inflict substantial impact forces. Here we demonstrate that dactyl impact surfaces consist of a finely-tuned mineral gradient, with fluorapatite substituting amorphous apatite towards the outer surface. Raman spectroscopy measurements show that calcium sulphate, previously not reported in mechanically active biotools, is co-localized with fluorapatite. Ab initio computations suggest that fluorapatite/calcium sulphate interfaces provide binding stability and promote the disordered-to-ordered transition of fluorapatite. Nanomechanical measurements show that fluorapatite crystalline orientation correlates with an anisotropic stiffness response and indicate significant differences in the fracture tolerance between the two types of appendages. Our findings shed new light on the crystallochemical and microstructural strategies allowing these intriguing biotools to optimize impact forces, providing physicochemical information that could be translated towards the synthesis of impact-resistant functional materials and coatings.
The structure of the stomatopod dactyl club--an ultrafast, hammer-like device used by the animal to shatter hard seashells--offers inspiration for impact-tolerant ceramics. Here, we present the micromechanical principles and related micromechanisms of deformation that impart the club with high impact tolerance. By using depth-sensing nanoindentation with spherical and sharp contact tips in combination with post-indentation residual stress mapping by Raman microspectroscopy, we show that the impact surface region of the dactyl club exhibits a quasi-plastic contact response associated with the interfacial sliding and rotation of fluorapatite nanorods, endowing the club with localized yielding. We also show that the subsurface layers exhibit strain hardening by microchannel densification, which provides additional dissipation of impact energy. Our findings suggest that the club's macroscopic size is below the critical size above which Hertzian brittle cracks are nucleated.
Creating a synthetic exoskeleton from abiotic materials to protect delicate mammalian cells and impart them with new functionalities could revolutionize fields like cell-based sensing and create diverse new cellular phenotypes. Herein, we introduce the concept of 'SupraCells', which are living mammalian cells encapsulated and protected within functional modular nanoparticle-based exoskeletons. Exoskeletons are generated within seconds through immediate interparticle and cell/particle complexation that abolishes the macropinocytotic and endocytotic nanoparticle internalization pathways that occur without complexation. SupraCell formation was shown to be generalizable to wide classes of nanoparticles and various types of cells. It induces a spore-like state, wherein cells do not replicate or spread on surfaces but are endowed with extremophile properties, e.g., resistance to osmotic stress, reactive oxygen species, pH, and UV exposure, along with abiotic properties like magnetism, conductivity, and multi-fluorescence. Upon de-complexation cells return to their normal replicative states. SupraCells represent a new class of living hybrid materials with a broad range of functionalities. Enhancing or augmenting the performance of mammalian cells could result in new classes of smart responsive living materials. Mammalian cells exhibit complex functionalities like sensing, signal transduction, and protein expression, but they remain fragile and highly susceptible to intracellular and extracellular stressors. [1] So far, to impart delicate mammalian cells with greater cellular durability, such as enhanced resistance against UV, freezing, and enzymatic attack, etc., a series of coating strategies/nanotechniques have been developed to
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