From biofilm and colony formation in bacteria to wound healing and embryonic development in multicellular organisms, groups of living cells must often move collectively. While considerable study has probed the biophysical mechanisms of how eukaryotic cells generate forces during migration, little such study has been devoted to bacteria, in particular with regard to the question of how bacteria generate and coordinate forces during collective motion. This question is addressed here for the first time using traction force microscopy. We study two distinct motility mechanisms of Myxococcus xanthus, namely twitching and gliding. For twitching, powered by type-IV pilus retraction, we find that individual cells exert local traction in small hotspots with forces on the order of 50 pN. Twitching of bacterial groups also produces traction hotspots, however with amplified forces around 100 pN. Although twitching groups migrate slowly as a whole, traction fluctuates rapidly on timescales <1.5 min. Gliding, the second motility mechanism, is driven by lateral transport of substrate adhesions. When cells are isolated, gliding produces low average traction on the order of 1 Pa. However, traction is amplified in groups by a factor of ~5. Since advancing protrusions of gliding cells push on average in the direction of motion, we infer a long-range compressive load sharing among sub-leading cells. Together, these results show that the forces generated during twitching and gliding have complementary characters and both forces are collectively amplified in groups.
Bacteria can spontaneously develop collective motions by aligning their motions in dense systems. Here, we show that bacteria can also respond collectively to an alternating electrical field and form dynamic clusters oscillating at the same frequency of the field. As the dynamic clusters go beyond a critical size, they split into smaller ones spontaneously. The critical size for splitting depends on the frequency of electric field and the concentration of bacteria. We show that instead of their biological activity, the physical properties of bacteria as charged particles are responsible for th…
Bacteria in bulk fluids swim collectively and display fascinating emergent dynamics. Although bacterial collective swimming in three-dimensional (3D) geometries has been well studied, its counterpart in confined two-dimensional (2D) geometries relevant to natural habitats of bacteria is still poorly understood. Here, through carefully designed experiments on Escherichia coli in Hele-Shaw chambers, we show that a small change in the degree of confinement leads to a drastic change in bacterial collective swimming. While long-range nematic order emerges for bacteria that can cross during encounte…
We have experimentally investigated the transitions of collective motions of bacterial cells in a shallow circular pool using the bacterial species $Bacillus$ $subtilis$. In our previous paper, we reported that the collective motions were classified into six phases on a phase diagram with two parameters, namely, the reduced cell length $λ$ and the cell density $ρ$. In this study, we focused on the sharp transitions at $λ\cong0.1$ ($\equiv λ_{\rm C1}$) with low values of $ρ$ between the $random$ $motion$ phase and the $one$-$way$ $rotational$ $motion$ phase. By introducing the order parameter $…
In systems as diverse as migrating mammals to road traffic, crowding acts to inhibit efficient collective movement. Bacteria, however, are observed to move in very dense groups containing billions of individuals without causing the gridlock common to other systems. Here we combine experiments, cell tracking and individual-based modelling to study the pathogen Pseudomonas aeruginosa as it collectively migrates across surfaces using grappling-hook like pili. We show that the fast moving cells of a hyperpilated mutant are overtaken and outcompeted by the slower moving wild-type at high cell densi…
We perform a bidimensional Stokes experiment in an active cellular material: an autonomously migrating monolayer of Madin-Darby Canine Kidney (MDCK) epithelial cells flows around a circular obstacle within a long and narrow channel, involving an interplay between cell shape changes and neighbour rearrangements. Based on image analysis of tissue flow and coarse-grained cell anisotropy, we determine the tissue strain rate, cell deformation and rearrangement rate fields, which are spatially heterogeneous. We find that the cell deformation and rearrangement rate fields correlate strongly, which is…
Cell migration plays essential roles in development, wound healing, diseases, and in the maintenance of a complex body. Experiments in collective cell migration generally measure quantities such as cell displacement and velocity. The observed short-time diffusion regime for mean square displacement in single-cell migration experiments on flat surfaces calls into question the definition of cell velocity and the measurement protocol. Theoretical results in stochastic modeling for single-cell migration have shown that this fast diffusive regime is explained by a white noise acting on displacement…
Tumor metastasis, traditionally considered as random spreading of individual cancer cells, has been shown to also involve coordinated collective invasion in the tissue space. Here we demonstrate experimentally and computationally that physical interactions between cells and extracellular matrix (ECM) support coordinated dissemination of cells from tumor organoids. We find that collective remodeling of the ECM fibrous structure by cell-generated forces produces reciprocal cues to bias cell motility. As a result, dissemination of cells from tumor organoids are controlled by the organoid geometry…
Living active collectives have evolved with remarkable self-patterning ability to meet the physical and biological constraints for growth and survival. However, how complex multicellular patterns emerge from a single founder cell remains elusive. Here, by recourse to an agent-based model, we track the three-dimensional (3D) morphodynamics and cell orientational order of growing bacterial biofilms encased by agarose gels. Confined growth causes spatiotemporally heterogeneous stress buildup in the biofilm. High hydrostatic and low shear stresses at the core of the biofilm promote viscous-to-elas…
In growing active matter systems, a large collection of engineered or living autonomous units metabolize free energy and create order at different length scales as they proliferate and migrate collectively. One such example is bacterial biofilms, which are surface-attached aggregates of bacterial cells embedded in an extracellular matrix. However, how bacterial growth coordinates with cell-surface interactions to create distinctive, long-range order in biofilms remains elusive. Here we report a collective cell reorientation cascade in growing Vibrio cholerae biofilms, leading to a differential…
Bacteria organize in a variety of collective states, from swarming, which has been attributed to rapid surface exploration, to biofilms, which are highly dense immobile communities attributed to stress resistance. It has been suggested that biofilm and swarming are oppositely controlled, making this transition particularly interesting for understanding the ability of bacterial colonies to adapt to challenging environments. Here, the swarm to biofilm transition is studied experimentally by analyzing the bacterial dynamics both on the individual and collective scales. We show that both biologica…
Many mature bacterial colonies and biofilms are complex three-dimensional (3D) structures. One key step in their developmental program is a transition from a two-dimensional (2D) monolayer into a 3D architecture. Despite the importance of controlling the growth of microbial colonies and biofilms in a variety of medical and industrial settings, the underlying physical mechanisms behind single-cell dynamics, collective behaviors of densely-packed cells, and 3D complex colony expansion remain largely unknown. In this work, we explore the mechanisms behind the 2D-to-3D transition of motile Pseudom…
Legionella are gram-negative, facultative intracellular, and pathogenic bacteria that pose a risk for human health and cause significant energy losses due to extensive preventive heating-up of water installations. We investigate acoustically-driven motion - acoustophoresis - of several Legionella species, Escherichia coli, Pseudomonas aeruginosa, and Acanthamoeba castellanii, a common Legionella host in water. All the investigated cells can be acoustically manipulated in an ultrasonic standing wave in water, as they possess a non-zero acoustic contrast that is positive for all of the cells, le…
Migrating cell clusters as active droplets with asymmetric shape and contact angles
Max Planck Institute for the Physics of Complex Systems（马克斯·普朗克复杂系统物理研究所）；Center for Systems Biology Dresden（德累斯顿系统生物学中心）；Cluster of Excellence Physics of Life, Technische Universität Dresden（德累斯顿工业大学生命物理卓越集群）；Departament de Física de la Matèria Condensada, Universitat de Barcelona（巴塞罗那大学凝聚态物理系）；Universitat de Barcelona Institute of Complex Systems (UBICS)（巴塞罗那大学复杂系统研究所）；Institució Catalana de Recerca i Estudis Avançats (ICREA)（加泰罗尼亚研究高级学院）
Soaring migrants exploit columns of rising air (thermals) to cover large distances with minimal energy. Employing social information while locating thermals may be beneficial, but examining collective movements in wild migrants has been a major challenge. We investigated the group movements of a flock of 27 naturally migrating, juvenile white storks using high-resolution GPS and accelerometers. Analyzing individual and group movements on multiple scales reveals that birds ahead navigate to and explore thermals, while followers benefit from their movements. Despite this benefit, followers often…
Active agents - like phoretic particles, bacteria, sperm, and cytoskeletal filaments in motility assays - show a large variety of motility-induced collective behaviors, such as aggregation, clustering and phase separation. The behavior of dense suspensions of phoretic particles and of bacteria during biofilm formation is determined by two principle physical mechanisms: (i) volume exclusion (short-range steric repulsion) and (ii) quorum sensing (longer-range reduced propulsion due to alteration of the local chemical environment). To systematically characterize such systems, we study semi-penetr…
We study the competition for space between two cell lines that differ only in the expression of the Ras oncogene. The two cell populations are initially separated and set to migrate antagonistically towards an in-between stripe of free substrate. After contact, their interface moves towards the population of normal cells. We interpret the velocity and traction force data taken before and after contact thanks to a hydrodynamic description of collectively migrating cohesive cell sheets. The kinematics of cells, before and after contact, allows us to estimate the relative material parameters for …
Shewanella oneidensis MR-1 are facultative aerobic electroactive bacteria, with an appealing potential for sustainable energy production and bioremediation. They gather around air sources, forming aerotactic bands and biofilms. Though accumulation is crucial to technological exploitation, their collective behaviour remains poorly reported. Here we establish a comprehensive framework for the study of aerotaxis, unveiling a novel hybrid locomotion pattern. Despite having only one flagellum, MR-1 combine motility features of mono- and multiflagellate bacteria, alternating longitudinal fast and si…
Collective cell migration in 3D extracellular matrix (ECM) is crucial to many physiological and pathological processes. Migrating cells can generate active pulling forces via actin filament contraction, which are transmitted to the ECM fibers and lead to a dynamically evolving force network in the system. Here, we elucidate the role of such force network in regulating collective cell behaviors using a minimal active-particle-on-network (APN) model, in which active particles can pull the fibers and hop between neighboring nodes of the network following local durotaxis. Our model reveals a dynam…
Collective migration -- the directed, coordinated motion of many self-propelled agents -- is a fascinating emergent behavior exhibited by active matter that has key functional implications for biological systems. Extensive studies have elucidated the different ways in which this phenomenon may arise. Nevertheless, how collective migration can persist when a population is confronted with perturbations, which inevitably arise in complex settings, is poorly understood. Here, by combining experiments and simulations, we describe a mechanism by which collectively migrating populations smooth out la…
The quest on how to collectively self-organize in order to maximize the survival chances of the members of a social group requires finding an optimal compromise between maximizing the well-being of an individual and that of the group. Here we develop a minimal model describing active individuals which consume or produce, and respond to a shared resource, such as the oxygen concentration for aerotactic bacteria or the temperature field for penguins, while urging for an optimal resource value. Notably, this model can be approximated by an attraction-repulsion model, but in general it features ma…
