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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.

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.

The teeth of all vertebrates predominantly comprise the same materials, but their lifespans vary widely: in stark contrast to mammals, shark teeth are functional only for weeks, rather than decades, making lifelong durability largely irrelevant. However, their diets are diverse and often mechanically demanding, and as such, their teeth should maintain a functional morphology, even in the face of extremely high and potentially damaging contact stresses. Here, we reconcile the dilemma between the need for an operative tooth geometry and the unavoidable damage inherent to feeding on hard foods, demonstrating that the tooth cusps of Port Jackson sharks, hard-shelled prey specialists, possess unusual microarchitecture that controls tooth erosion in a way that maintains functional cusp shape. The graded architecture in the enameloid provokes a location-specific damage response, combining chipping of outer enameloid and smooth wear of inner enameloid to preserve an efficient shape for grasping hard prey. Our discovery provides experimental support for the dominant theory that multi-layered tooth enameloid facilitated evolutionary diversification of shark ecologies. Shark teeth have short lifespans yet can be subject to significant mechanical damage. Here, the authors report on a site-specific damage mechanism in shark teeth enameloid, which maintains tooth functional shape, providing experimental evidence that tooth architecture may have influenced the diversification of shark ecologies over evolution.

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. Interfacial water constitutes a formidable barrier to strong surface bonding, hampering the development of water-resistant synthetic adhesives. Here, the authors elucidate the precise time-regulated secretion of mussel adhesive proteins in Perna viridis , probing their surface structures and subsequent roles.

While hierarchical ordering is a distinctive feature of natural tissues and is directly responsible for their diverse and unique properties, efforts to synthesize biomaterials have primarily focused on using molecular-based approaches with little emphasis on multiscale structure. Here, we report a bottom-up self-assembly process to produce highly porous hydrogel fibers that resemble extracellular matrices both structurally and mechanically. Physically crosslinked nanostructured micelles form the walls of micrometer-sized water-rich pores with preferred orientation along the fiber direction. Low elastic moduli (<1 kPa), high elasticity (extending by more than 12 times the initial length), non-linear elasticity (e.g., hyperelasticity), and completely reversible extension are derived from unevenly distributed strain between the micrometer-sized pores and the polymer chains, which is reminiscent of cellular solids. Control of the material microstructure and orientation over many orders of magnitude (e.g., nm–μm), while holding the nanostructure constant, reveals how the multiscale structure directly impacts mechanical properties. Hierarchical ordering is critical for preparing biomimetic materials, but control of multiscale structure over many length scales is limited. Here, the authors report on a bottom-up assembly process for producing highly porous hydrogel structures where structure dictates bulk properties.

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.

The movement of valves of bivalved invertebrates is enabled through the action of muscles and the interplay between the muscles and the hinge ligament. The muscles that move the valves attach to their internal surface. To promote the structural integrity at the mechanically mismatched interfaces, a specific crystal microstructure and texture are present at the muscle attachment sites. These are different from the crystal microstructure and texture of the rest of the valves. We present here for modern two- and three-layered brachiopod shells (Magellania venosa, Liothyrella neozelanica and Gryphus vitreus) the mode of crystal organisation at sites of adductor and diductor muscle attachments (i) relative to the microstructure and texture that forms the other sections of the valves and (ii) relative to crystal organisation of muscle attachment sites of bivalved invertebrates of other phyla, namely, species of the class Bivalvia. We discuss similarities/differences in Ca-carbonate phase, microstructure and texture between rhynchonellate brachiopods and bivalves, and discuss whether the Ca-carbonate crystal organisation of muscle attachment sites is convergent for bivalved marine organisms. We show significant differences in muscle attachment site architecture and highlight the different structural solutions developed by nature for shells of marine organisms that serve the same purpose.

Despite the economic and ecological importance of corals’ skeletal structure, as well as their predicted vulnerability to future climate change, few studies have examined the skeletal mechanical properties at the nanoscale. As climate change is predicted to alter coral growth and physiology, as well as increase mechanical stress events (e.g., bioerosion, storm frequency), it is crucial to understand how skeletal mechanical properties change with environmental conditions. Moreover, while material properties are intimately linked to the chemical composition of the skeleton, no previous study has examined mechanical properties alongside carbonate geochemical composition. Using Porites coral cores from a wide range of reef environments (Thailand, Singapore, Taiwan), we correlated coral’s micro-mechanical properties with chemical composition. In contrast to previous mechanical measurements of reef-building corals, we document unprecedented variability in the hardness, stiffness, and micro-cracking stress of Porites corals across reef environments, which may significantly decrease the structural integrity of reef substrate. Corals from environments with low salinity and high sedimentation had higher organic content and fractured at lower loads, suggesting that skeletal organic content caused enhanced embrittlement. Within individual coral cores, we observed seasonal variability in skeletal stiffness, and a relationship between high sea surface temperature, increased stiffness, and high-density. Regionally, lower Sr/Ca and higher Mg/Ca coincided with decreased stiffness and hardness, which is likely driven by increased amorphous calcium carbonate and skeletal organic content. If the coral is significantly embrittled, as measured here in samples from Singapore, faster erosion is expected. A decrease in skeletal stiffness will decrease the quality of reef substrate, enhance the rate of bioerosion by predators and borers, and increase colony dislodgement, resulting in widespread loss of structural complexity.

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. Nanoindentation and spectroscopy measurements show that the impact surface of the dactyl club—a hammer-like device that stomatopods use to shatter hard seashells—has a quasi-plastic response that enhances the damage tolerance of the clubs.

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 raptorial appendages of stomatopods are known to inflict large impact forces at high speeds, while exhibiting large damage tolerance. Here, the authors study the structure, distribution and nanomechanical properties of mineral phases in stomatopod's clubs, finding that calcium sulphate is co-localized with crystalline fluorapatite.