Physics of self-rolling viruses.

Viruses are right at the interface of inanimate matter and life. However, recent experiments [Sakai et al., J. Virol. 92, e01522-17 (2018)0022-538X10.1128/JVI.01522-17] have shown that some influenza strains can actively roll on glycan-covered surfaces. In a previous letter [Ziebert and Kulic, Phys. Rev. Lett. 126, 218101 (2021)0031-900710.1103/PhysRevLett.126.218101] we suggested this to be a form of viral surface metabolism: a collection of spike proteins that attach to and cut the glycans act as a self-organized mechano-chemical motor. Here we study in more depth the physics of the emergent self-rolling states. We give scaling arguments how the motion arises, substantiated by a detailed analytical theory that yields the full torque-angular velocity relation of the self-organized motor. Stochastic Gillespie simulations are used to validate the theory and to quantify stochastic effects like virus detachment and reversals of its direction. Finally, we also cross-check several approximations made previously and show that the proposed mechanism is very robust. All these results point together to the statistical inevitability of viral rolling in the presence of enzymatic activity.

How Influenza's Spike Motor Works.

While often believed to be a passive agent that merely exploits its host's metabolism, the influenza virus has recently been shown to actively move across glycan-coated surfaces. This form of enzymatically driven surface motility is currently not well understood and has been loosely linked to burnt-bridge Brownian ratchet mechanisms. Starting from known properties of influenza's spike proteins, we develop a physical model that quantitatively describes the observed motility. It predicts a collectively emerging dynamics of spike proteins and surface-bound ligands that combined with the virus' geometry give rise to a self-organized rolling propulsion. We show that in contrast to a Brownian ratchet, the rotary spike drive is not fluctuation driven but operates optimally as a macroscopic engine in the deterministic regime. The mechanism also applies to relatives of influenza and to man-made analogs like DNA monowheels and should give guidelines for their optimization.

Dynamics of fiberboids.

Fiberboids are active filaments trapped at the interface of two phases, able of harnessing energy (and matter) fluxes across the interface in order to produce a rolling-like self-propulsion. We discuss several table-top examples and develop the physical framework for understanding their complex dynamics. In spite of some specific features in the examples studied we conclude that the phenomenon of fiberboids is highly generic and robust across different materials, types of fluxes and timescales. Fiberboid motility should play a role from the macroscopic realm down to the micro scale and, as recently hypothesized, possibly as a means of biological self-propulsion that has escaped previous attention.

Helical Superstructure of Intermediate Filaments.

Intermediate filaments are the least explored among the large cytoskeletal elements. We show here that they display conformational anomalies in narrow microfluidic channels. Their unusual behavior can be understood as the consequence of a previously undetected, large-scale helically curved superstructure. Confinement in a channel orders the otherwise soft, strongly fluctuating helical filaments and enhances their structural correlations, giving rise to experimentally detectable, strongly oscillating tangent correlation functions. We propose an explanation for the detected intrinsic curving phenomenon-an elastic shape instability that we call autocoiling. The mechanism involves self-induced filament buckling via a surface stress located at the outside of the cross section. The results agree with ultrastructural findings and rationalize for the commonly observed looped intermediate filament shapes. Beyond curvature, explaining the molecular origin of the detected helical torsion remains an interesting challenge.

Motorizing fibres with geometric zero-energy modes.

Responsive materials1-3 have been used to generate structures with built-in complex geometries4-6, linear actuators7-9 and microswimmers10-12. These results suggest that complex, fully functional machines composed solely from shape-changing materials might be possible 13 . Nonetheless, to accomplish rotary motion in these materials still relies on the classical wheel and axle motifs. Here we explore geometric zero-energy modes to elicit rotary motion in elastic materials in the absence of a rigid wheel travelling around an axle. We show that prestrained polymer fibres closed into rings exhibit self-actuation and continuous motion when placed between two heat baths due to elastic deformations that arise from rotational-symmetry breaking around the rod's axis. Our findings illustrate a simple but robust model to create active motion in mechanically prestrained objects.

Resonant reshaping of colloidal clusters on a current carrying wire.

Colloids in confined geometries promise a path towards tailored microscopic superstructures. Yet, a major roadblock is posed by kinetically trapped states that prevent the assemblies from reaching their anticipated shapes. We investigate magnetic colloids trapped on a cylindrical surface of a current carrying wire. If kinetic traps could be avoided the wire's surface would act as an ideal mold for colloidal rings and helical fibers. We devise here a way to dynamically shake down the clusters and avoid kinetic traps in their energy landscape. A low frequency magnetic modulation wave around the wire axis effectively eliminates defects from the clusters and stretches them into slender rings and helical filaments. A theoretical model is developed that qualitatively explains the observed resonant reshaping response of clusters.

Squeezed helical elastica.

We theoretically study the conformations of a helical semi-flexible filament confined to a flat surface. This squeezed helix exhibits a variety of unexpected shapes resembling circles, waves or spirals depending on the material parameters. We explore the conformation space in detail and show that the shapes can be understood as the mutual elastic interaction of conformational quasi-particles. Our theoretical results are potentially useful to determine the material parameters of such helical filaments in an experimental setting.

How bio-filaments twist membranes.

We study the deformations of a fluid membrane imposed by adhering stiff bio-filaments due to the torques they apply. In the limit of small deformations, we derive a general expression for the energy and the deformation field of the membrane. This expression is specialised to different important cases including closed and helical bio-filaments. In particular, we analyse interface-mediated interactions and membrane wrapping when the filaments apply a local torque distribution on a tubular membrane.

A nonequilibrium power balance relation for analyzing dissipative filament dynamics.

Biofilaments like F-actin or microtubules, as well as cilia, flagella, or filament bundles, are often deformed by distributed and time-dependent external forces. It is highly desirable to characterize these filaments' mechanics in an efficient way, either using a single experiment or a high throughput method. We here propose a dynamic power balance approach to study nonequilibrium filament dynamics and exemplify it both experimentally and theoretically by applying it to microtubule gliding assay dynamics. Its usefulness is highlighted by the experimental determination of the lateral friction coefficient for microtubules on kinesins. In contrast to what is usually assumed, friction is anisotropic, in a similar fashion as hydrodynamic friction. We also exemplify, by considering a microtubule buckling event, that if at least one parameter is known in advance, all other parameters can be determined by analyzing a single time-dependent experiment.

Why microtubules run in circles: mechanical hysteresis of the tubulin lattice.

The fate of every eukaryotic cell subtly relies on the exceptional mechanical properties of microtubules. Despite significant efforts, understanding their unusual mechanics remains elusive. One persistent, unresolved mystery is the formation of long-lived arcs and rings, e.g., in kinesin-driven gliding assays. To elucidate their physical origin we develop a model of the inner workings of the microtubule's lattice, based on recent experimental evidence for a conformational switch of the tubulin dimer. We show that the microtubule lattice itself coexists in discrete polymorphic states. Metastable curved states can be induced via a mechanical hysteresis involving torques and forces typical of few molecular motors acting in unison, in agreement with the observations.

Topological energy storage of work generated by nanomotors.

Most macroscopic machines rely on wheels and gears. Yet, rigid gears are entirely impractical on the nano-scale. Here we propose a more useful method to couple any rotary engine to any other mechanical elements on the nano- and micro-scale. We argue that a rotary molecular motor attached to an entangled polymer energy storage unit, which together form what we call the "tanglotron" device, is a viable concept that can be experimentally implemented. We derive the torque-entanglement relationship for a tanglotron (its "equation of state") and show that it can be understood by simple statistical mechanics arguments. We find that a typical entanglement at low packing density costs around 6kT. In the high entanglement regime, the free energy diverges logarithmically close to a maximal geometric packing density. We outline several promising applications of the tanglotron idea and conclude that the transmission, storage and back-conversion of topological entanglement energy are not only physically feasible but also practical for a number of reasons.

Confotronic dynamics of tubular filaments.

Tubular lattices are ubiquitous in nature and technology. Microtubules and nanotubes of all kinds act as important pillars of biological cells and the man-made nano-world. We show that when prestress is introduced in such structures, localized conformational quasiparticles emerge and govern the collective shape dynamics of the lattice. When coupled via cooperative interactions these quasiparticles form larger-scale quasipolymer superstructures exhibiting collective dynamic modes and giving rise to a hallmark behavior radically different from semiflexible beams.

Theory of coherent van der Waals matter.

We explain in depth the previously proposed theory of the coherent van der Waals (cvdW) interaction, the counterpart of van der Waals (vdW) force, emerging in spatially coherently fluctuating electromagnetic fields. We show that cvdW driven matter is dominated by many-body interactions, which are significantly stronger than those found in standard van der Waals (vdW) systems. Remarkably, the leading two- and three-body interactions are of the same order with respect to the distance (∝R(-6)), in contrast to the usually weak vdW three-body effects (∝R(-9)). From a microscopic theory we show that the anisotropic cvdW many-body interactions drive the formation of low-dimensional structures such as chains, membranes, and vesicles with very unusual, nonlocal properties. In particular, cvdW chains display a logarithmically growing stiffness with the chain length, while cvdW membranes have a bending modulus growing linearly with their size. We argue that the cvdW anisotropic many-body forces cause local cohesion but also a negative effective "surface tension." We conclude by deriving the equation of state for cvdW materials and propose experiments to test the theory, in particular the unusual three-body nature of cvdW.

Self-assembly of colloidal superstructures in coherently fluctuating fields.

From microscopic fluid clusters to macroscopic droplets, the structure of fluids is governed by the van der Waals force, a force that acts between polarizable objects. In this Letter, we derive a general theory that describes the nonequilibrium counterpart to the van der Waals force, which emerges in spatially coherently fluctuating electromagnetic fields. We describe the formation of a novel and complex hierarchy of self-organized morphologies in magnetic and dielectric colloid systems. Most striking among these morphologies are dipolar foams--colloidal superstructures that swell against gravity and display a high sensitivity to the applied field. We discuss the dominance of many-body forces and derive the equation of state for a material formed by the coherent van der Waals force. Our theory is applied to recent experiments in paramagnetic colloidal systems and a new experiment is suggested to test the theory.

Solvable model for polymorphic dynamics of biofilaments.

We investigate an analytically tractable toy model for thermally induced polymorphic dynamics of cooperatively rearranging biofilaments-like microtubules. The proposed four-block model, which can be seen as a coarse-grained approximation of the full polymorphic tube model, permits a complete analytical treatment of all thermodynamic properties including correlation functions and angular Fourier mode distributions. Due to its mathematical tractability the model straightforwardly leads to some physical insights in recently discussed phenomena like the "length dependent persistence length." We show that a polymorphic filament can disguise itself as a classical worm-like chain on small and on large scales and yet display distinct anomalous tell-tale features indicating an inner switching dynamics on intermediate length scales.

Cooperative lattice dynamics and anomalous fluctuations of microtubules.

Microtubules have been in the focus of biophysical research for several decades. However, the confusing and mutually contradictory results regarding their elasticity and fluctuations have cast doubt on their present understanding. In this paper, we present the empirical evidence for the existence of discrete guanosine diphosphate (GDP)-tubulin fluctuations between a curved and a straight configuration at room temperature as well as for conformational tubulin cooperativity. Guided by a number of experimental findings, we build the case for a novel microtubule model, with the principal result that microtubules can spontaneously form micron-sized cooperative helical states with unique elastic and dynamic features. The polymorphic dynamics of the microtubule lattice resulting from the tubulin bistability quantitatively explains several experimental puzzles, including anomalous scaling of dynamic fluctuations of grafted microtubules, their apparent length-stiffness relation, and their remarkable curved-helical appearance in general. We point out that the multistability and cooperative switching of tubulin dimers could participate in important cellular processes, and could in particular lead to efficient mechanochemical signaling along single microtubules.

Tubulin bistability and polymorphic dynamics of microtubules.

Based on the hypothesis that the GDP-tubulin dimer is a conformationally bistable molecule-rapidly fluctuating between a discrete curved and a straight state-we develop a model for polymorphic dynamics of the microtubule lattice. We show that GDP-tubulin bistability consistently explains unusual dynamic fluctuations, the apparent length-stiffness relation of grafted taxol-stabilized microtubules, and the curved-helical appearance of microtubules in general. When clamped by one end the microtubules undergo an unusual zero energy motion-in its effect reminiscent of a limited rotational hinge. We conclude that microtubules exist in highly cooperative energy-degenerate helical states and discuss possible implications in vivo.

The role of microtubule movement in bidirectional organelle transport.

We study the role of microtubule movement in bidirectional organelle transport in Drosophila S2 cells and show that EGFP-tagged peroxisomes in cells serve as sensitive probes of motor induced, noisy cytoskeletal motions. Multiple peroxisomes move in unison over large time windows and show correlations with microtubule tip positions, indicating rapid microtubule fluctuations in the longitudinal direction. We report the first high-resolution measurement of longitudinal microtubule fluctuations performed by tracing such pairs of co-moving peroxisomes. The resulting picture shows that motor-dependent longitudinal microtubule oscillations contribute significantly to cargo movement along microtubules. Thus, contrary to the conventional view, organelle transport cannot be described solely in terms of cargo movement along stationary microtubule tracks, but instead includes a strong contribution from the movement of the tracks.

Equation of state of looped DNA.

We derive the equation of state of DNA under tension that features a loop. Such loops occur transiently during DNA condensation in the presence of multivalent ions or permanently through sliding protein linkers such as condensin. The force-extension relation of such looped-DNA modeled as a wormlike chain is calculated via path integration in the semiclassical limit. This allows us to rigorously determine the high stretching asymptotics. Notably the functional form of the force-extension curve resembles that of straight DNA, yet with a strongly renormalized apparent persistence length. We also present analogous results for DNA under tension with several protein-induced kinks and/or loops. That means that the experimentally extracted single-molecule elasticity does not necessarily only reflect the bare DNA stiffness, but can also contain additional contributions that depend on the overall chain conformation and length.

Motor driven microtubule shape fluctuations: force from within the lattice.

We develop a general theory of microtubule (MT) deformations by molecular motors generating internal force doublets within the MT lattice. We describe two basic internal excitations, the S and V shape, and compare them with experimental observations from literature. We explain the special role of tubulin vacancies and the dramatic deformation amplifying effect observed for katanin acting at positions of defects. Experimentally observed shapes are used to determine the ratio of MT stretch and shear moduli (approximately 6 x 10(5)) and to estimate the forces induced in the MT lattice by katanin (10's of pN). We conclude that molecular motors if acting cooperatively can "animate" MTs from within the lattice and induce slack even without cross bridging to other structures, a scenario very much reminiscent of the motor driven axoneme.