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Collective cell dynamics is essential for tissue morphogenesis and various biological functions. However, it remains incompletely understood how mechanical forces and chemical signaling are integrated to direct collective cell behaviors underlying tissue morphogenesis. Here, we propose a three-dimensional (3D) mechanochemical theory accounting for biochemical reaction-diffusion and cellular mechanotransduction to investigate the dynamics of multicellular lumens. We show that the interplay between biochemical signaling and mechanics can trigger either pitchfork or Hopf bifurcation to induce diverse static mechanochemical patterns or generate oscillations with multiple modes both involving marked mechanical deformations in lumens. We uncover the crucial role of mechanochemical feedback in emerging morphodynamics and identify the evolution and morphogenetic functions of hierarchical topological defects including cell-level hexatic defects and tissue-level orientational defects. Our theory captures the common mechanochemical traits of collective dynamics observed in experiments and could provide a mechanistic context for understanding morphological symmetry breaking in 3D lumen-like tissues.
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Mecanotransducción Celular , Modelos Biológicos , Morfogénesis , Fenómenos Biomecánicos , AnimalesRESUMEN
Actomyosin networks constrict cell area and junctions to alter cell and tissue shape. However, during cell expansion under mechanical stress, actomyosin networks are strengthened and polarized to relax stress. Thus, cells face a conflicting situation between the enhanced actomyosin contractile properties and the expansion behaviour of the cell or tissue. To address this paradoxical situation, we study late Drosophila oogenesis and reveal an unusual epithelial expansion wave behaviour. Mechanistically, Rac1 and Rho1 integrate basal pulsatile actomyosin networks with ruffles and focal adhesions to increase and then stabilize basal area of epithelial cells allowing their flattening and elongation. This epithelial expansion behaviour bridges cell changes to oocyte growth and extension, while oocyte growth in turn deforms the epithelium to drive cell spreading. Basal pulsatile actomyosin networks exhibit non-contractile mechanics, non-linear structures and F-actin/Myosin-II spatiotemporal signal separation, implicating unreported expanding properties. Biophysical modelling incorporating these expanding properties well simulates epithelial cell expansion waves. Our work thus highlights actomyosin expanding properties as a key mechanism driving tissue morphogenesis.
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Actomiosina , Proteínas de Drosophila , Animales , Actomiosina/metabolismo , Proteínas de Drosophila/metabolismo , Células Epiteliales/metabolismo , Citoesqueleto de Actina/metabolismo , Drosophila/metabolismo , Epitelio/metabolismo , MorfogénesisRESUMEN
The interfacial interactions between epithelia and cancer cells have profound relevance for tumor development and metastasis. Through monolayer confrontation of MCF10A (nontumorigenic human breast epithelial cells) and MDA-MB-231 (human epithelial breast cancer cells) cells, we investigate the epithelial-cancerous interfacial interactions at the tissue level. We show that the monolayer interaction leads to competitive interfacial morphodynamics and drives an intricate spatial organization of MCF10A cells into multicellular finger-like structures, which further branch into multiple subfinger-like structures. These hierarchical interfacial structures penetrate the cancer monolayer and can spontaneously segregate or even envelop cancer cell clusters, consistent with our theoretical prediction. By tracking the substrate displacements via embedded fluorescent nanobeads and implementing nanomechanical modeling that combines atomic force microscopy and finite element simulations, we computed mechanical force patterns, including traction forces and monolayer stresses, caused by the monolayer interaction. It is found that the heterogeneous mechanical forces accumulated in the monolayers are able to squeeze cancer cells, leading to three-dimensional interfacial bulges or cell extrusion, initiating the p53 apoptosis signaling pathways of cancer cells. We reveal that intercellular E-cadherin and P-cadherin of epithelial cells differentially regulate the interfacial organization including migration speed, directionality, spatial correlation, F-actin alignment, and subcellular protrusions of MCF10A cells; whereas E-cadherin governs interfacial geometry that is relevant to force localization and cancer cell extrusion, P-cadherin maintains interfacial integrity that enables long-range force transmission. Our findings suggest that the collaborative molecular and mechanical behaviors are crucial for preventing epithelial tissues from undergoing tumor invasion.
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Cadherinas , Neoplasias , Humanos , Cadherinas/metabolismo , Actinas/metabolismo , Células Epiteliales/metabolismo , Adhesión CelularRESUMEN
The left-right symmetry breaking of vertebrate embryos requires nodal flow. However, the molecular mechanisms that mediate the asymmetric gene expression regulation under nodal flow remain elusive. Here, we report that heat shock factor 1 (HSF1) is asymmetrically activated in the Kupffer's vesicle of zebrafish embryos in the presence of nodal flow. Deficiency in HSF1 expression caused a significant situs inversus and disrupted gene expression asymmetry of nodal signaling proteins in zebrafish embryos. Further studies demonstrated that HSF1 is a mechanosensitive protein. The mechanical sensation ability of HSF1 is conserved in a variety of mechanical stimuli in different cell types. Moreover, cilia and Ca2+-Akt signaling axis are essential for the activation of HSF1 under mechanical stress in vitro and in vivo. Considering the conserved expression of HSF1 in organisms, these findings unveil a fundamental mechanism of gene expression regulation by mechanical clues during embryonic development and other physiological and pathological transformations.
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Understanding the principles underlying the self-organization of stem cells into tissues is fundamental for deciphering human embryo development. Here, we report that, without three-dimensional (3D) extracellular matrix (ECM) overlay, human pluripotent stem cells (hPSCs) cultured on two-dimensional soft elastic substrates can self-organize into 3D cysts resembling the human epiblast sac in a stiffness-dependent manner. Our theoretical modeling predicts that this cyst organization is facilitated and guided by the spontaneous nesting of the soft substrate, which results from the adhesion-dependent mechanical interaction between cells and substrate. Such substrate nesting is sufficient for the 3D assembly and polarization of hPSCs required for cyst organization, even without 3D ECM overlay. Furthermore, we identify that the reversible substrate nesting and cyst morphogenesis also require appropriate activation of ROCK-Myosin II pathway. This indicates a unique set of tissue morphomechanical signaling mechanisms that clearly differ from the canonical cystogenic mechanism previously reported in 3D ECM. Our findings highlight an unanticipated synergy between mechanical microenvironment and mechanotransduction in controlling tissue morphogenesis and suggest a mechanics-based strategy for generation of hPSCs-derived models for early human embryogenesis. STATEMENT OF SIGNIFICANCE: Soft substrates can induce the self-organization of human pluripotent stem cells (hPSCs) into cysts without three-dimensional (3D) extracellular matrix (ECM) overlay. However, the underlying mechanisms by which soft substrate guides cystogenesis are largely unknown. This study shows that substrate nesting, resulting from cell-substrate interaction, plays an important role in cyst organization, including 3D assembly and apical-basal polarization. Additionally, actomyosin contractility mediated by the ROCK-Myosin II pathway also contributes to the substrate deformation and cyst morphology. These findings demonstrate the interplay between the mechanical microenvironment and cells in tissue morphogenesis, suggesting a mechanics-based strategy in building hPSC-derived models for early human embryo development.
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Cells migrate by adapting their leading-edge behaviors to heterogeneous extracellular microenvironments (ECMs) during cancer invasions and immune responses. Yet it remains poorly understood how such complicated dynamic behaviors emerge from millisecond-scale assembling activities of protein molecules, which are hard to probe experimentally. To address this gap, we establish a spatiotemporal "resistance-adaptive propulsion" theory based on the interactions between Arp2/3 complexes and polymerizing actin filaments and a multiscale dynamic modeling system spanning from molecular proteins to the cell. We quantitatively find that cells can accurately self-adapt propulsive forces to overcome heterogeneous ECMs via a resistance-triggered positive feedback mechanism, dominated by polymerization-induced actin filament bending and the bending-regulated actin-Arp2/3 binding. However, for high resistance regions, resistance triggers a negative feedback, hindering branched filament assembly, which adapts cellular morphologies to circumnavigate the obstacles. Strikingly, the synergy of the two opposite feedbacks not only empowers the cell with both powerful and flexible migratory capabilities to deal with complex ECMs but also enables efficient utilization of intracellular proteins by the cell. In addition, we identify that the nature of cell migration velocity depending on ECM history stems from the inherent temporal hysteresis of cytoskeleton remodeling. We also show that directional cell migration is dictated by the competition between the local stiffness of ECMs and the local polymerizing rate of actin network caused by chemotactic cues. Our results reveal that it is the polymerization force-regulated actin filament-Arp2/3 complex binding interaction that dominates self-adaptive cell migrations in complex ECMs, and we provide a predictive theory and a spatiotemporal multiscale modeling system at the protein level.
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Citoesqueleto de Actina , Actinas , Polimerizacion , Movimiento Celular , Citoesqueleto , Complejo 2-3 Proteico Relacionado con la ActinaRESUMEN
The morphology and motion behavior of a cell are highly influenced by its external biological, chemical, and physical stimuli, and geometric confinement. In this paper, it is revealed that the mean curvature of the substrate significantly influences the adhesion of vesicles. By employing the variational method and investigating the Helfrich free energy, the configuration of axisymmetric vesicles adhered to curved spherical substrates is obtained theoretically. Moreover, numerical simulations based on the finite element method are also carried out to investigate the adhesion of vesicles on curved substrates with complex shapes. It is found that for a fixed area of a vesicle, its total free energy depends mainly on the mean curvature of the adhesion region but is insensitive to the specific shape of the substrate, and the total free energy monotonically decreases with the increase in the mean curvature. In addition, possible biological significances of the curvature-dependent adhesion, such as the shape of the cell and antibiofouling, are discussed. This study may deepen our understanding of the underlying mechanisms of adhesion in cellular activities.
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Bacteria adapt the mechanical properties of their cell envelope, including cell wall stiffness, turgor, and cell wall tension and deformation, to grow and survive in harsh environments. However, it remains a technical challenge to simultaneously determine these mechanical properties at a single cell level. Here we combined theoretical modelling with an experimental approach to quantify the mechanical properties and turgor of Staphylococcus epidermidis. It was found that high osmolarity leads to a decrease in both cell wall stiffness and turgor. We also demonstrated that the turgor change is associated with a change in the viscosity of the bacterial cell. We predicted that the cell wall tension is much higher in deionized (DI) water and it decreases with an increase in osmolality. We also found that an external force increases the cell wall deformation to reinforce its adherence to a surface and this effect can be more significant in lower osmolarity. Overall, our work highlights how bacterial mechanics supports survival in harsh environments and uncovers the adaption of bacterial cell wall mechanical integrity and turgor to osmotic and mechanical challenges.
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Bacterias , Pared Celular , Microscopía de Fuerza Atómica , Pared Celular/metabolismo , Membrana Celular , Presión OsmóticaRESUMEN
Human brain experiences vibration of certain magnitude and frequency during various physical activities such as vehicle transportation and machine operation, which may cause traumatic brain injury or other brain diseases. However, the mechanisms of brain pathogenesis due to vibration are not fully elucidated due to the lack of techniques to study brain functions while applying vibration to the brain at a specific magnitude and frequency. Here, this study reported a custom-built head-worn electromagnetic actuator that applied vibration to the brain in vivo at an accurate frequency inside a magnetic resonance imaging scanner while cerebral blood flow (CBF) was acquired. Using this technique, CBF values from 45 healthy volunteers were quantitatively measured immediately following vibration at 20, 30, 40 Hz, respectively. Results showed increasingly reduced CBF with increasing frequency at multiple regions of the brain, while the size of the regions expanded. Importantly, the vibration-induced CBF reduction regions largely fell inside the brain's default mode network (DMN), with about 58 or 46% overlap at 30 or 40 Hz, respectively. These findings demonstrate that vibration as a mechanical stimulus can change strain conditions, which may induce CBF reduction in the brain with regional differences in a frequency-dependent manner. Furthermore, the overlap between vibration-induced CBF reduction regions and DMN suggested a potential relationship between external mechanical stimuli and cognitive functions.
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Encéfalo , Vibración , Humanos , Imagen por Resonancia Magnética , Cognición , Circulación Cerebrovascular/fisiologíaRESUMEN
The growth of biological tissues, which is regulated by a variety of factors, can induce stresses that may, in turn, destabilize the tissues into diverse patterns. In most previous studies, however, tissue growth was usually assumed as a prescribed parameter independent of stresses, limiting our understanding of the mechanobiological morphogenesis of real tissues. In this paper, we propose a theoretical model to investigate the mechanobiological response of soft tissues undergoing stress-modulated growth. Linear stability analysis is first performed to elucidate the surface instability mechanism induced by stress-modulated volumetric growth. We further conduct finite element simulations to validate the theoretical prediction and, particularly, to capture the post-buckling pattern evolution. Our results show that the non-uniform stresses, which evolve with the tissue growth and morphogenesis, exert mechanical feedback on the growth itself, producing up-down asymmetric surface morphologies as observed in, for example, the gyrification of human brains and brain organoids. It is also revealed that large residual stresses are unnecessary to cause mechanobiological instability and subsequent asymmetric patterning, which has long been believed to be driven by sufficiently high stresses. The present work could help us to understand the morphological changes of biological tissues under physiological and pathological conditions.
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Modelos Biológicos , Modelos Teóricos , Humanos , Morfogénesis , Estrés Mecánico , Análisis de Elementos FinitosRESUMEN
Morphogenesis of active shells such as cells is a fundamental chemomechanical process that often exhibits three-dimensional (3D) large deformations and chemical pattern dynamics simultaneously. Here, we establish a chemomechanical active shell theory accounting for mechanical feedback and biochemical regulation to investigate the symmetry-breaking and 3D chiral morphodynamics emerging in the cell cortex. The active bending and stretching of the elastic shells are regulated by biochemical signals like actomyosin and RhoA, which, in turn, exert mechanical feedback on the biochemical events via deformation-dependent diffusion and inhibition. We show that active deformations can trigger chemomechanical bifurcations, yielding pulse spiral waves and global oscillations, which, with increasing mechanical feedback, give way to traveling or standing waves subsequently. Mechanical feedback is also found to contribute to stabilizing the polarity of emerging patterns, thus ensuring robust morphogenesis. Our results reproduce and unravel the experimentally observed solitary and multiple spiral patterns, which initiate asymmetric cleavage in Xenopus and starfish embryogenesis. This study underscores the crucial roles of mechanical feedback in cell development and also suggests a chemomechanical framework allowing for 3D large deformation and chemical signaling to explore complex morphogenesis in living shell-like structures.
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Fenómenos Químicos , Citoesqueleto de Actina , Actomiosina , Diferenciación Celular , Química Física , MorfogénesisRESUMEN
Mechanical nociception is an evolutionarily conserved sensory process required for the survival of living organisms. Previous studies have revealed much about the neural circuits and sensory molecules in mechanical nociception, but the cellular mechanisms adopted by nociceptors in force detection remain elusive. To address this issue, we study the mechanosensation of a fly larval nociceptor (class IV da neurons, c4da) using a customized mechanical device. We find that c4da are sensitive to mN-scale forces and make uniform responses to the forces applied at different dendritic regions. Moreover, c4da showed a greater sensitivity to localized forces, consistent with them being able to detect the poking of sharp objects, such as wasp ovipositor. Further analysis reveals that high morphological complexity, mechanosensitivity to lateral tension and possibly also active signal propagation in dendrites contribute to the sensory features of c4da. In particular, we discover that Piezo and Ppk1/Ppk26, two key mechanosensory molecules, make differential but additive contributions to the mechanosensitivity of c4da. In all, our results provide updates into understanding how c4da process mechanical signals at the cellular level and reveal the contributions of key molecules.
Being able to sense harm is essential for survival. Animals have to be able to tell the difference between a gentle touch and a dangerous pressure. They do this using nerve cells called mechanical nociceptors which switch on when the body feels a potentially painful pressure, such as a sharp object poking the skin. Once activated, the nerves send outputs to other parts of the central nervous system which coordinate the motions needed to escape the source of the pain. One popular model to understand harm-sensing is the larvae of fruit flies which automatically roll back and forth when they sense the pointy sting of a wasp. This process is initiated by sensory nerve cells called class IV dendritic arborization neurons (or c4da for short) which sit under the fly's skin. However, it is still not fully understood how these mechanical nociceptors detect the poking forces of the wasp's tail. To investigate, Liu, Wu et al. built a device that could poke sections of fly larvae under a microscope so they could see how different types of pressure affected the activity and shape of c4da cells. This revealed that c4da nerves were most sensitive to sharp objects that illicit a more localized force, which may explain why these cells are so good at responding to wasp attacks. Further analysis showed that this sensitivity was due to the high number of branches, or dendrites, protruding from the body of c4da nerves. Liu, Wu et al. discovered that the dendrites were coated in a touch-sensitive protein that can sense and amplify both squashing and pulling, resulting in a signal that activates c4da nerves to send outputs to other parts of the central nervous system. This mechanism increases the likelihood that a c4da cell will detect a mechanical pressure even if it is far away from the body of the nerve. These findings shed light on how sensory cells like c4da are optimized to carry out specific roles. This could be important for understanding other nerve systems which sense mechanical pressure, such as those involved in touch or auditory processes. However, further work is needed to see whether the molecules and mechanism identified by Liu, Wu et al. are also present in humans.
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Proteínas de Drosophila , Drosophila , Animales , Drosophila/metabolismo , Nociceptores/metabolismo , Proteínas de Drosophila/metabolismo , Drosophila melanogaster/fisiología , Larva/fisiología , Canales Iónicos , Canales Epiteliales de SodioRESUMEN
Phase transitions are common in inanimate systems and have been studied extensively in natural sciences. Less explored are the rich transitions that take place at the micro- and nano-scales in biological systems. In conventional phase transitions, large-scale properties of the media change discontinuously in response to continuous changes in external conditions. Such changes play a significant role in the dynamic behaviours of organisms. In this review, we focus on some transitions in both free-living and biofilms of bacteria. Particular attention is paid to the transitions in the flagellar motors and filaments of free-living bacteria, in cellular gene expression during the biofilm growth, in the biofilm morphology transitions during biofilm expansion, and in the cell motion pattern transitions during the biofilm formation. We analyse the dynamic characteristics and biophysical mechanisms of these phase transition phenomena and point out the parallels between these transitions and conventional phase transitions. We also discuss the applications of some theoretical and numerical methods, established for conventional phase transitions in inanimate systems, in bacterial biofilms.
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Bacterias , Biopelículas , Bacterias/metabolismoRESUMEN
Growing axons are one-dimensional active structures that are important for wiring the brain and repairing nerves. However, the biophysical mechanisms underlying the complex kinetics of growing axons remain elusive. Here, we develop a theoretical framework to recapitulate force-regulated states and their transitions in growing axons. We demonstrate a unique negative feedback mechanism that defines four distinct kinetic states in a growing axon, whose transitional boundaries depend on the interplay between cytoskeletal dynamics and axon-substrate adhesion. A phase diagram for axonal growth is formulated based on two dimensionless numbers.
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Axones , Encéfalo , Axones/fisiologíaRESUMEN
A falling liquid drop, after impact on a rigid substrate, deforms and spreads, owing to the normal reaction force. Subsequently, if the substrate is nonwetting, the drop retracts and then jumps off. As we show here, not only is the impact itself associated with a distinct peak in the temporal evolution of the normal force, but also the jump-off, which was hitherto unknown. We characterize both peaks and elucidate how they relate to the different stages of the drop impact process. The time at which the second peak appears coincides with the formation of a Worthington jet, emerging through flow focusing. Even low-velocity impacts can lead to a surprisingly high second peak in the normal force, even larger than the first one, namely when the Worthington jet becomes singular due to the collapse of an air cavity in the drop.
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Rigidity of the extracellular matrix markedly regulates many cellular processes. However, how cells detect and respond to matrix rigidity remains incompletely understood. Here, we propose a unified two-dimensional multiscale framework accounting for the chemomechanical feedback to explore the interrelated cellular mechanosensing, polarization, and migration, which constitute the dynamic cascade in cellular response to matrix stiffness but are often modeled separately in previous theories. By combining integrin dynamics and intracellular force transduction, we show that substrate stiffness can act as a switch to activate or deactivate cell polarization. Our theory quantitatively reproduces rich stiffness-dependent cellular dynamics, including spreading, polarity selection, migration pattern, durotaxis, and even negative durotaxis, reported in a wide spectrum of cell types, and reconciles some inconsistent experimental observations. We find that a specific bipolarized mode can determine the optimal substrate stiffness, which enables the fastest cell migration rather than the largest traction forces that cells apply on the substrate. We identify that such a mechanical adaptation stems from the force balance across the whole cell. These findings could yield universal insights into various stiffness-mediated cellular processes within the context of tissue morphogenesis, wound healing, and cancer invasion.
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Matriz Extracelular , Adhesiones Focales , Movimiento Celular , Matriz Extracelular/metabolismo , Adhesiones Focales/metabolismo , Integrinas/metabolismo , Fenómenos Mecánicos , Mecanotransducción CelularRESUMEN
The growth and development of biological tissues and organs strongly depend on the requirements of their multiple functions. Plant veins yield efficient nutrient transport and withstand various external loads. Victoria cruziana, a tropical species of the Nymphaeaceae family of water lilies, has evolved a network of three-dimensional and rugged veins, which yields a superior load-bearing capacity. However, it remains elusive how biological and mechanical factors affect their unique vein layout. In this paper, we propose a multi-functional and large-scale topology optimization method to investigate the morphomechanics of Victoria cruziana veins, which optimizes both the structural stiffness and nutrient transport efficiency. Our results suggest that increasing the branching order of radial veins improves the efficiency of nutrient delivery, and the gradient variation of circumferential vein sizes significantly contributes to the stiffness of the leaf. In the present method, we also consider the optimization of the wall thickness and the maximum layout distance of circumferential veins. Furthermore, biomimetic leaves are fabricated by using the three-dimensional printing technique to verify our theoretical findings. This work not only gains insights into the morphomechanics of Victoria cruziana veins, but also helps the design of, for example, rib-reinforced shells, slabs and dome skeletons.
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Nymphaeaceae , Hojas de la Planta , Plantas , Soporte de PesoRESUMEN
Using atomic force microscopy, we have shown that friction on graphene/h-BN superlattice structures may exhibit unusual moiré-scale stick slip in addition to the regular ones observed at the atomic scale. Such dual-scale slip instability will lead to unique length-scale dependent energy dissipation when the different slip mechanisms are sequentially activated. Assisted by an improved theoretical model and comparative experiments, we find that accumulation and unstable release of the in-plane strain of the graphene layer is the key mechanism underlying the moiré-scale behavior. This work highlights the distinct role of the internal state of the van der Waals interfaces in determining the rich dynamics and energy dissipation of layer-structured materials.
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Atomic reconstruction has been widely observed in two-dimensional van der Waals structures with small twist angles1-7. This unusual behaviour leads to many novel phenomena, including strong electronic correlation, spontaneous ferromagnetism and topologically protected states1,5,8-14. Nevertheless, atomic reconstruction typically occurs spontaneously, exhibiting only one single stable state. Using conductive atomic force microscopy, here we show that, for small-angle twisted monolayer-multilayer graphene, there exist two metastable reconstruction states with distinct stacking orders and strain soliton structures. More importantly, we demonstrate that these two reconstruction states can be reversibly switched, and the switching can propagate spontaneously in an unusual domino-like fashion. Assisted by lattice-resolved conductive atomic force microscopy imaging and atomistic simulations, the detailed structure of the strain soliton networks has been identified and the associated propagation mechanism is attributed to the strong mechanical coupling among solitons. The fine structure of the bistable states is critical for understanding the unique properties of van der Waals structures with tiny twists, and the switching mechanism offers a viable means for manipulating their stacking states.
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Grafito , Electrónica , Grafito/químicaRESUMEN
As a species of insects living on water, water striders jump from the water surface to avoid predation and then steadily land without piercing the surface. This spectacular property has attracted extensive interests since it provides bio-inspirations for designing functional microrobots moving on water. In this work, we investigate the landing dynamics of water striders by using artificial striders with different masses and leg lengths. It is found that once a water strider has landed, it oscillates on the water surface and the amplitude decays gradually, triggering a sequence of surface waves. Through scaling analysis, we relate the depth of the dimple that the strider leg displaces to its landing velocity, as well as its leg length and body mass. The subsequent time evolution of the interface where the strider lands is modeled as a damped oscillator, and its energy is exhausted by the surface waves. Moreover, we discuss the maximum depth of the dimple excited by the landing and find that the dynamic process can store more energy than the statically deforming process. Finally, we put forward a criterion of piercing the water surface from the energy point of view. These findings should be of great importance for understanding the locomotion of insects on water and for designing robust water-walking bionic robots.