The mussel byssus stem provides a strong and compact mechanically mismatched biointerface between living tissue and a nonliving biopolymer. Yet, in a poorly understood process, mussels can simply ...jettison their entire byssus, rebuilding a new one in just hours. We characterized the structure and composition of the byssus biointerface using histology, confocal Raman mapping, phase contrast–enhanced microcomputed tomography, and advanced electron microscopy, revealing a sophisticated junction consisting of abiotic biopolymer sheets interdigitated between living extracellular matrix. The sheet surfaces are in intimate adhesive contact with billions of motile epithelial cilia that control biointerface strength and stem release through their collective movement, which is regulated neurochemically. We posit that this may involve a complex sensory pathway by which sessile mussels respond to environmental stresses to release and relocate.
Editor’s summary
There are many strategies in nature and biomedicine for establishing strong connections between living tissue and nonliving surfaces, but the mechanisms for separating these biointerfaces quickly and on demand are less well understood.
Mytilus
mussels can strongly adhere to inorganic surfaces, but they can also rapidly detach when threatened. Sivasundarampillai
et al
. use advanced imaging and spectroscopy methods to study the detachment process (see the Perspective by Pan and Li). They found that the responsiveness of this quick release relies on the oscillating motion of cilia and subsequently the change of mechanical interaction between the byssus stem and mussel foot tissues. The beating movement can be influenced by the application of serotonin and dopamine, thus implicating neurotransmitters in controlling the mechanical interaction between living and nonliving tissues. —Marc S. Lavine
Mussels create a quick-release interface between living and nonliving material with neurochemically regulated strength.
Biology offers a valuable inspiration toward the development of self-healing engineering composites and polymers. In particular, chemical level design principles extracted from proteinaceous ...biopolymers, especially the mussel byssus, provide inspiration for design of autonomous and intrinsic healing in synthetic polymers. The mussel byssus is an acellular tissue comprised of extremely tough protein-based fibers, produced by mussels to secure attachment on rocky surfaces. Threads exhibit self-healing response following an apparent plastic yield event, recovering initial material properties in a time-dependent fashion. Recent biochemical analysis of the structure-function relationships defining this response reveal a key role of sacrificial cross-links based on metal coordination bonds between Zn
ions and histidine amino acid residues. Inspired by this example, many research groups have developed self-healing polymeric materials based on histidine (imidazole)-metal chemistry. In this review, we provide a detailed overview of the current understanding of the self-healing mechanism in byssal threads, and an overview of the current state of the art in histidine- and imidazole-based synthetic polymers.
Marine mussels (Mytilus edulis) fabricate byssal threads, high-performance biopolymeric fibers, which exhibit exceptional toughness and self-healing capacity. These properties are associated with ...collagenous proteins in the fibrous thread core known as preCols that self-organize into a hierarchical semicrystalline structure. Threads assemble individually in a bottom-up process lasting just minutes via secretion of membrane bound vesicles filled with preCols. However, very little is understood about the details and dynamics of this assembly process. Here, we explore the hypothesis that preCols are stored within the vesicles in a liquid crystalline phase, which contributes to fiber assembly by preordering molecules. To achieve this, a protocol was developed for extracting and isolating intact preCol secretory vesicles in high yield and purity. Vesicles were characterized and were manipulated in vitro, clearly indicating the dynamic liquid crystalline nature of the proteins within. Moreover, mechanical shearing of vesicles led to formation of highly birefringent preCol fibers. These findings have relevance for efforts toward sustainable production of advanced polymeric materials, and possibly for engineering biomedical scaffolds based on collagenous proteins.
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IJS, KILJ, NUK, PNG, UL, UM
Velvet worms eject a fluid capture slime that can be mechanically drawn into stiff biopolymeric fibres. Remarkably, these fibres can be dissolved by extended exposure to water, and new regenerated ...fibres can be drawn from the dissolved fibre solution-indicating a fully recyclable process. Here, we perform a multiscale structural and compositional investigation of this reversible fabrication process with the velvet worm Euperipatoides rowelli, revealing that biopolymeric fibre assembly is facilitated via mono-disperse lipid-protein nanoglobules. Shear forces cause nanoglobules to self-assemble into nano- and microfibrils, which can be drawn into macroscopic fibres with a protein-enriched core and lipid-rich coating. Fibre dissolution in water leads to re-formation of nanoglobules, suggesting that this dynamic supramolecular assembly of mechanoresponsive protein-building blocks is mediated by reversible non-covalent interactions. These findings offer important mechanistic insights into the role of mechanochemical processes in bio-fibre formation, providing potential avenues for sustainable material fabrication processes.Velvet worms expel a fluid slime that, under shear force, forms stiff fibres that can be dissolved and then regenerated. Here, the authors reveal that the recyclability of these biopolymers relies on mechanoresponsive lipid-protein nanoglobules in the slime that reversibly self-assemble into fibrils.
For prey capture and defense, velvet worms eject an adhesive slime which has been established as a model system for recyclable complex liquids. Triggered by mechanical agitation, the liquid ...bio‐adhesive rapidly transitions into solid fibers. In order to understand this mechanoresponsive behavior, here, the nanostructural organization of slime components are studied using small‐angle scattering with neutrons and X‐rays. The scattering intensities are successfully described with a three‐component model accounting for proteins of two dominant molecular weight fractions and nanoscale globules. In contrast to the previous assumption that high molecular weight proteins—the presumed building blocks of the fiber core—are contained in the nanoglobules, it is found that the majority of slime proteins exist freely in solution. Only less than 10% of the slime proteins are contained in the nanoglobules, necessitating a reassessment of their function in fiber formation. Comparing scattering data of slime re‐hydrated with light and heavy water reveals that the majority of lipids in slime are contained in the nanoglobules with homogeneous distribution. Vibrating mechanical impact under exclusion of air neither leads to formation of fibers nor alters the bulk structure of slime significantly, suggesting that interfacial phenomena and directional shearing are required for fiber formation.
Small‐angle neutron scattering reveals the nanoscale organization of velvet worm slime. The rapid, mechanically induced transition of this liquid bioadhesive into stiff fibers is based on the self‐assembly of proteins that are freely localized in solution. Nanoglobules, the previously assumed storage units for these fiber precursors, only contain small amounts of proteins and lipids.
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BFBNIB, FZAB, GIS, IJS, KILJ, NLZOH, NUK, OILJ, SBCE, SBMB, UL, UM, UPUK
The adhesive plaques of Mytilus byssus are investigated increasingly to determine the molecular requirements for wet adhesion. Mfp-2 is the most abundant protein in the plaques, but little is known ...about its function. Analysis of Mfp-2 films using the surface forces apparatus detected no interaction between films or between a film and bare mica; however, addition of Ca2+ and Fe3+ induced significant reversible bridging (work of adhesion Wad ≈ 0.3 mJ/m2 to 2.2 mJ/m2) between two films at 0.35 m salinity. The strongest observed Fe3+-mediated bridging approaches the adhesion of oriented avidin-biotin complexes. Raman microscopy of plaque sections supports the co-localization of Mfp-2 and iron, which interact by forming bis- or tris-DOPA-iron complexes. Mfp-2 adhered strongly to Mfp-5, a DOPA-rich interfacial adhesive protein, but not to another interfacial protein, Mfp-3, which may in fact displace Mfp-2 from mica. In the presence of metal ions or Mfp-5, Mfp-2 adhesion was fully reversible. These results suggest that plaque cohesiveness depends on Mfp-2 complexation of metal ions, particularly Fe3+ and also by Mfp-2 interaction with Mfp-5 at the plaque-substratum interface.
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GEOZS, IJS, IMTLJ, KILJ, KISLJ, NLZOH, NUK, OILJ, PNG, SAZU, SBCE, SBJE, UILJ, UL, UM, UPCLJ, UPUK, ZAGLJ, ZRSKP
Over the last 15 years, the byssus of marine mussels (Mytilus spp.) has emerged as an important model system for the bio-inspired development and synthesis of advanced polymers and adhesives. But how ...did these seemingly inconsequential fibers that are routinely discarded in mussel hors d’oeuvres become the focus of intense international research. In the present review, we take a historical perspective to understand this phenomenon. Our purpose is not to review the sizeable literature of mussel-inspired materials, as there are numerous excellent reviews that cover this topic in great depth. Instead, we explore how the byssus became a magnet for bio-inspired materials science, with a focus on the specific breakthroughs in the understanding of composition, structure, function, and formation of the byssus achieved through fundamental scientific investigation. Extracted principles have led to bio-inspired design of novel materials with both biomedical and technical applications, including surgical adhesives, self-healing polymers, tunable hydrogels, and even actuated composites. Continued study into the byssus of Mytilid mussels and other species will provide a rich source of inspiration for years to come.
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DOBA, IZUM, KILJ, NUK, PILJ, PNG, SAZU, SIK, UILJ, UKNU, UL, UM, UPUK
The mucilaginous viscin tissue within mistletoe berries possesses an extraordinary ability to be rapidly processed under ambient conditions into stiff cellulosic fibers (>14 GPa) through simple ...mechanical drawing. This rapid and extreme transformation process is hydration-dependent and involves an astonishing >200-fold increase in length, providing a relevant role model for efforts to produce advanced composites from cellulose-based structures such as cellulose nanocrystals or cellulose nanofibrils. Using a combination of in situ polarized light microscopy, synchrotron X-ray scattering, and humidity-controlled mechanical analysis, we examine here the dynamic transition of a viscin cell bundle from hydrogel-like tissues to high-performance fibers. Our findings indicate a massive phase transition in which cellulose microfibrils containing high-aspect-ratio crystalline domains undergo dramatic reorganization, facilitated by a water-responsive noncellulosic matrix. Transition from an aligned, yet flowing state to a stiff fiber is likely triggered by rapid water loss below 45% relative humidity. These findings not only help understanding the adaptive success of mistletoe but may also be relevant for the development of new facile processing methods for next-generation cellulosic composites.
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IJS, KILJ, NUK, PNG, UL, UM
Mussels (Mytilus edulis) adhere to hard surfaces in intertidal marine habitats with a porous underwater glue called the byssus plaque. The plaque is an established role model for bioinspired ...underwater glues and comprises at least six proteins, most of which are highly cationic and enriched in the post-translationally modified amino acid 3,4-dihydroxyphenylalanine (DOPA). While much is known about the chemistry of plaque adhesion, less is understood about the natural plaque formation process. Here, we investigated plaque structure and formation using 3D electron microscopic imaging, revealing that micro- and nanopores form spontaneously during secretion of protein-filled secretory vesicles. To better understand this process, we developed a method to purify intact secretory vesicles for in vitro assembly studies. We discovered that each vesicle contains a sulfate-associated fluid condensate consisting of ∼9 histidine- and/or DOPA-rich proteins, which are presumably the required ingredients for building a plaque. Rupturing vesicles under specific buffering conditions relevant for natural assembly led to controlled multiphase liquid–liquid phase separation (LLPS) of different proteins, resulting in formation of a continuous phase with coexisting droplets. Rapid coarsening of the droplet phase was arrested through pH-dependent cross-linking of the continuous phase, producing native-like solid porous “microplaques” with droplet proteins remaining as fluid condensates within the pores. Results indicate that histidine deprotonation and sulfates figure prominently in condensate cross-linking. Distilled concepts suggest that combining phase separation with tunable cross-linking kinetics could be effective for microfabricating hierarchically porous materials via self-assembly.
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IJS, KILJ, NUK, PNG, UL, UM
The objective is to determine how the COVID-19 pandemic affected care for patients undergoing thoracic surgery for cancer.
The COVID-19 pandemic accelerated the adoption of telemedicine.
...Characteristics and outcomes of new patients seen between March 1 and June 30, 2019, and the same period in 2020 were compared. Patients who did not undergo surgery were excluded. Patients who had a telemedicine visit (new and established) in the 2020 period were asked to complete a survey.
In total, 624 new patients were seen in 2019 versus 299 in 2020 (52% reduction); 45% of patients (n=136) in 2020 were seen via telemedicine. There was no statistically significant difference in time to surgery, pathological upstaging, or postsurgical complications between 2019 and 2020. In total, 1085 patients (new and established) had a telemedicine visit in 2020; 239 (22%) completed the survey. A majority replied that telemedicine was equivalent to in-person care (77%), did not impair care quality (84%), resulted in less stress (69%) and shorter waits (86%), was more convenient (92%), saved money and commuting time (93%), and expanded who could attend visits (91%). Some patients regretted the loss of human interaction (71%). Most would opt for telemedicine after the pandemic (60%), although some would prefer in-person format for initial visits (55%) and visits with complex discussions (49%). Only 21% were uncomfortable with the telemedicine technology.
Telemedicine enabled cancer care to continue during the COVID-19 pandemic without delays in surgery, cancer progression, or worsened postoperative morbidity and was generally well received.
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