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Collective motion and swarming
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Bacterial-surfaces interactions
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Complex dynamics of marine bacteria
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Competitions between microorganisms
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Our lab combines a large variety of physical approaches, wet-lab biological based experiments, mathematical modeling, precise and innovative microscopy and three dimensional particle tracking methods. We study intricate collective phenomena in nature. For instance, we ask why do bacteria swarm, what are the mechanisms involved during swarming, and what are the evolutionary advantages of swarming?
3D swarming analysis; implications for antibiotics tolerance
Swarming bacteria are an example of a complex, active biological system, where high cell density and super-diffusive cell mobility confer survival advantages to the group as a whole. Previous studies on the dynamics of the swarm have been limited to easily observable regions at the advancing edge of the swarm where cells are restricted to a plane. In this study, using defocused epifluorescence video imaging, we have tracked the motion of fluorescently labeled individuals within the interior of a densely packed three-dimensional (3D) region of a swarm. Our analysis reveals a novel 3D architecture, where bacteria are constrained by inter-particle interactions, sandwiched between two distinct boundary conditions. We find that secreted biosurfactants keep bacteria away from the swarm-air upper boundary, and added antibiotics at the lower swarm-surface boundary lead to their migration away from this boundary. Formation of the antibiotic-avoidance zone is dependent on a functional chemotaxis signaling system, in the absence of which the swarm loses its high tolerance to the antibiotics.
Role of tumbling in bacterial swarming
Typical wild-type bacteria swimming in sparse suspensions exhibit a movement pattern called run-and-tumble, characterized by straight trajectories (“runs”) interspersed by shorter random reorientation (“tumbles”). This is achieved by rotating their flagella counterclockwise, or clockwise, respectively. The chemotaxis signaling network operates in controlling the frequency of tumbles, enabling navigation towards or away from desired regions in the medium. In contrast, while in dense populations, flagellated bacteria exhibit collective motion and form large dynamic clusters, whirls and jets, with intricate dynamics that is fundamentally different than trajectories of sparsely swimming cells. Although collectively swarming cells do change direction at the level of the individual cell, often exhibiting reversals, it has been suggested that chemotaxis does not play a role in multicellular colony expansion, but the change in direction is stemming from clockwise flagellar rotation. In this work, the effects of cell rotor switching (i.e., the ability to tumble) and chemotaxis on the collective statistics of swarming bacteria are studied experimentally in wild-type Bacillus subtilis and two mutants – one that does not tumble and one that tumbles independent of the chemotaxis system. We show that while several of the parameters examined are similar between the strains, other collective and individual characteristics are significantly different. The results demonstrate that tumbling and/or flagellar directional rotor switching has an important role on the dynamics of swarming, and imply that swarming models of self-propelled rods that do not take tumbling and/or rotor switching into account may be over-simplified.
Chaotic model for Lévy walks in swarming bacteria
We describe a new mechanism for Lévy walks, explaining the recently observed super-diffusion of swarming bacteria. The model hinges on several key physical properties of bacteria, such as an elongated cell shape, self-propulsion and a collectively generated regular vortex-like flow. In particular, chaos and Levy walking are a consequence of group dynamics. The model explains how cells can fine-tune the geometric properties of their trajectories. Experiments confirm the spectrum of these patterns in fluorescently labeled swarming Bacillus subtilis.
Effect of cell aspect ratio on swarming bacteria
Swarming bacteria collectively migrate on surfaces using flagella, forming dynamic whirls and jets that consist of millions of individuals. Because some swarming bacteria elongate prior to actual motion, cell aspect ratio may play a significant role in the collective dynamics. Extensive research on self-propelled rod-like particles confirms that elongation promotes alignment, strongly affecting the dynamics. Here, we study experimentally the collective dynamics of variants of swarming {\it Bacillus subtilis}, that differ in length. We show that the swarming statistics depends on aspect ratio in a critical, fundamental fashion not predicted by theory. The fastest motion was obtained for the wild-type and variants that are similar in length. However, shorter and longer cells exhibit anomalous, non-Gaussian statistics and non-exponential decay of the auto-correlation function, indicating lower collective motility. These results suggest that the robust mechanisms to maintain aspect ratios may be important for efficient swarming motility. Wild-type cells are optimal in this sense.
Swarming bacteria move against their own flow
Simultaneous acquisition of phase-contrast light microscopy and fluorescently-labeled bacteria, moving within a dense swarm, reveals the intricate interactions between cells and the collective flow around them. By comparing wild type and immotile cells embedded in a dense wild type swarm, the effect of the active thrust generated by the flagella can be singled out. It is shown that while the distribution of angles between cell velocity, cell orientation and the local flow around it is Gaussian-like for immotile bacteria, wild type cells exhibit anomalous non-Gaussian deviations and are able to move in trajectories perpendicular to the collective flow. Thus, cells can maneuver or switch between local streams and jets. A minimal model describing bacteria as hydrodynamic force dipoles shows that steric effects, hydrodynamics interactions and local alignments all have to be taken into account in order to explain the observed dynamics. These findings shed light on the physical mechanisms underlying bacterial swarming and the balance between individual and collective dynamics.
Swarming bacteria migrate by Lévy walk
Individual swimming bacteria are known to bias their random trajectories in search of food and to optimize survival. The motion of bacteria within a swarm, wherein they migrate as a collective group over a solid surface, is fundamentally different as typical bacterial swarms show large-scale swirling and streaming motions involving millions to billions of cells. Here, by tracking trajectories of fluorescently labeled individuals within such dense swarms, we find that the bacteria are performing super-diffusion, consistent with Lévy walks. Lévy walks are characterized by trajectories that have straight stretches for extended lengths whose variance is infinite. The evidence of super-diffusion consistent with Lévy walks in bacteria suggests that this strategy may have evolved considerably earlier than previously thought.
Antibiotic-Induced Anomalous Statistics of Collective Bacterial Swarming
Under sublethal antibiotics concentrations, the statistics of collectively swarming Bacillus subtilis transitions from normal to anomalous, with a heavy-tailed speed distribution and a two-step temporal correlation of velocities. The transition is due to changes in the properties of the bacterial motion and the formation of a motility-defective subpopulation that self-segregates into regions. As a result, both the colonial expansion and the growth rate are not affected by antibiotics. This phenomenon suggests a new strategy bacteria employ to fight antibiotic stress.
Collective motion of spherical bacteria
A large variety of motile bacterial species exhibit collective motions while inhabiting liquids or colonizing surfaces. These collective motions are often characterized by coherent dynamic clusters, where hundreds of cells move in correlated whirls and jets. Previously, all species that were known to form such motion had a rod-shaped structure, which enhances the order through steric and hydrodynamic interactions. Here we show that the spherical motile bacteria Serratia marcescens exhibit robust collective dynamics and correlated coherent motion while grown in suspensions. As cells migrate to the upper surface of a drop, they form a monolayer, and move collectively in whirls and jets. At all concentrations, the distribution of the bacterial speed was approximately Rayleigh with an average that depends on concentration in a non-monotonic way. Other dynamical parameters such as vorticity and correlation functions are also analyzed and compared to rod-shaped bacteria from the same strain. Our results demonstrate that self-propelled spherical objects do form complex ordered collective motion. This opens a door for a new perspective on the role of cell aspect ratio and alignment of cells with regards to collective motion in nature.
Some on the dynamics of marine bacteria
Trichodesmium spp. are diazotrophic cyanobacteria that exist as single filaments (trichomes) and as macroscopic colonies of varying shapes formed by aggregating trichomes. The causes and dynamics of colony formation and disassociation are not yet elucidated. We demonstrate that limited availability of dissolved phosphorus (P) or iron (Fe) stimulated trichome mobility and induced colony formation in Trichodesmium erythraeum IMS101 cultures. The specific nutrient limitation differentially affected the rate of colony formation and morphology of the colonies. Fe starvation promoted rapid colony formation (10–48 h from depletion) while 5–7 days were required for colonies to form in P-depleted cultures. Video analyses confirmed that the probability of trichomes to cluster increased from 12 to 35% when transferred from nutrient replete to Fe depleted conditions. Moreover, the probability for Fe-depleted aggregates to remain colonial increased to 50% from only 10% in nutrient replete cultures. These colonies were also characterized by stronger attachment forces between the trichomes. Enrichment of nutrient-depleted cultures with the limited nutrient-stimulated colony dissociation into single trichomes. We postulate that limited P and Fe availability enhance colony formation of Trichodesmium and primarily control the abundance and distribution of its different morphologies in the nutrient-limited surface ocean.
Competition between colonies
Bacteria can secrete a wide array of antibacterial compounds when competing with other bacteria for the same resources. Some of these compounds, such as bacteriocins, can affect bacteria of similar or closely related strains. In some cases, these secretions have been found to kill sibling cells that belong to the same colony. Here, we present experimental observations of competition between 2 sibling colonies of Paenibacillus dendritiformis grown on a low-nutrient agar gel. We find that neighboring colonies (growing from droplet inoculation) mutually inhibit growth through secretions that become lethal if the level exceeds a well-defined threshold. In contrast, within a single colony developing from a droplet inoculation, no growth inhibition is observed. However, growth inhibition and cell death are observed if material extracted from the agar between 2 growing colonies is introduced outside a growing single colony. To interpret the observations, we devised a simple mathematical model for the secretion of an antibacterial compound. Simulations of this model illustrate how secretions from neighboring colonies can be deadly, whereas secretions from a single colony growing from a droplet are not.
Collective dynamics of long bacteria
Bacterial swarming is a type of motility characterized by a rapid and collective migration of bacteria on surfaces. Most swarming species form densely packed dynamic clusters in the form of whirls and jets, in which hundreds of rod-shaped rigid cells move in circular and straight patterns, respectively. Recent studies have suggested that short-range steric interactions may dominate hydrodynamic interactions and that geometrical factors, such as a cell’s aspect ratio, play an important role in bacterial swarming. Typically, the aspect ratio for most swarming species is only up to 5, and a detailed understanding of the role of much larger aspect ratios remains an open challenge. Here we study the dynamics of Paenibacillus dendritiformis C morphotype, a very long, hyperflagellated, straight (rigid), rod-shaped bacterium with an aspect ratio of20. We find that instead of swarming in whirls and jets as observed in most species, including the shorter T morphotype of P. dendritiformis, the C morphotype moves in densely packed straight but thin long lines. Within these lines, all bacteria show periodic reversals, with a typical reversal time of 20 s, which is independent of their neighbors, the initial nutrient level, agar rigidity, surfactant addition, humidity level, temperature, nutrient chemotaxis, oxygen level, illumination intensity or gradient, and cell length. The evolutionary advantage of this unique back-and-forth surface translocation remains unclear.
Swarming bacteria are an example of a complex, active biological system, where high cell density and super-diffusive cell mobility confer survival advantages to the group as a whole. Previous studies on the dynamics of the swarm have been limited to easily observable regions at the advancing edge of the swarm where cells are restricted to a plane. In this study, using defocused epifluorescence video imaging, we have tracked the motion of fluorescently labeled individuals within the interior of a densely packed three-dimensional (3D) region of a swarm. Our analysis reveals a novel 3D architecture, where bacteria are constrained by inter-particle interactions, sandwiched between two distinct boundary conditions. We find that secreted biosurfactants keep bacteria away from the swarm-air upper boundary, and added antibiotics at the lower swarm-surface boundary lead to their migration away from this boundary. Formation of the antibiotic-avoidance zone is dependent on a functional chemotaxis signaling system, in the absence of which the swarm loses its high tolerance to the antibiotics.
Role of tumbling in bacterial swarming
Typical wild-type bacteria swimming in sparse suspensions exhibit a movement pattern called run-and-tumble, characterized by straight trajectories (“runs”) interspersed by shorter random reorientation (“tumbles”). This is achieved by rotating their flagella counterclockwise, or clockwise, respectively. The chemotaxis signaling network operates in controlling the frequency of tumbles, enabling navigation towards or away from desired regions in the medium. In contrast, while in dense populations, flagellated bacteria exhibit collective motion and form large dynamic clusters, whirls and jets, with intricate dynamics that is fundamentally different than trajectories of sparsely swimming cells. Although collectively swarming cells do change direction at the level of the individual cell, often exhibiting reversals, it has been suggested that chemotaxis does not play a role in multicellular colony expansion, but the change in direction is stemming from clockwise flagellar rotation. In this work, the effects of cell rotor switching (i.e., the ability to tumble) and chemotaxis on the collective statistics of swarming bacteria are studied experimentally in wild-type Bacillus subtilis and two mutants – one that does not tumble and one that tumbles independent of the chemotaxis system. We show that while several of the parameters examined are similar between the strains, other collective and individual characteristics are significantly different. The results demonstrate that tumbling and/or flagellar directional rotor switching has an important role on the dynamics of swarming, and imply that swarming models of self-propelled rods that do not take tumbling and/or rotor switching into account may be over-simplified.
Chaotic model for Lévy walks in swarming bacteria
We describe a new mechanism for Lévy walks, explaining the recently observed super-diffusion of swarming bacteria. The model hinges on several key physical properties of bacteria, such as an elongated cell shape, self-propulsion and a collectively generated regular vortex-like flow. In particular, chaos and Levy walking are a consequence of group dynamics. The model explains how cells can fine-tune the geometric properties of their trajectories. Experiments confirm the spectrum of these patterns in fluorescently labeled swarming Bacillus subtilis.
Effect of cell aspect ratio on swarming bacteria
Swarming bacteria collectively migrate on surfaces using flagella, forming dynamic whirls and jets that consist of millions of individuals. Because some swarming bacteria elongate prior to actual motion, cell aspect ratio may play a significant role in the collective dynamics. Extensive research on self-propelled rod-like particles confirms that elongation promotes alignment, strongly affecting the dynamics. Here, we study experimentally the collective dynamics of variants of swarming {\it Bacillus subtilis}, that differ in length. We show that the swarming statistics depends on aspect ratio in a critical, fundamental fashion not predicted by theory. The fastest motion was obtained for the wild-type and variants that are similar in length. However, shorter and longer cells exhibit anomalous, non-Gaussian statistics and non-exponential decay of the auto-correlation function, indicating lower collective motility. These results suggest that the robust mechanisms to maintain aspect ratios may be important for efficient swarming motility. Wild-type cells are optimal in this sense.
Swarming bacteria move against their own flow
Simultaneous acquisition of phase-contrast light microscopy and fluorescently-labeled bacteria, moving within a dense swarm, reveals the intricate interactions between cells and the collective flow around them. By comparing wild type and immotile cells embedded in a dense wild type swarm, the effect of the active thrust generated by the flagella can be singled out. It is shown that while the distribution of angles between cell velocity, cell orientation and the local flow around it is Gaussian-like for immotile bacteria, wild type cells exhibit anomalous non-Gaussian deviations and are able to move in trajectories perpendicular to the collective flow. Thus, cells can maneuver or switch between local streams and jets. A minimal model describing bacteria as hydrodynamic force dipoles shows that steric effects, hydrodynamics interactions and local alignments all have to be taken into account in order to explain the observed dynamics. These findings shed light on the physical mechanisms underlying bacterial swarming and the balance between individual and collective dynamics.
Swarming bacteria migrate by Lévy walk
Individual swimming bacteria are known to bias their random trajectories in search of food and to optimize survival. The motion of bacteria within a swarm, wherein they migrate as a collective group over a solid surface, is fundamentally different as typical bacterial swarms show large-scale swirling and streaming motions involving millions to billions of cells. Here, by tracking trajectories of fluorescently labeled individuals within such dense swarms, we find that the bacteria are performing super-diffusion, consistent with Lévy walks. Lévy walks are characterized by trajectories that have straight stretches for extended lengths whose variance is infinite. The evidence of super-diffusion consistent with Lévy walks in bacteria suggests that this strategy may have evolved considerably earlier than previously thought.
Antibiotic-Induced Anomalous Statistics of Collective Bacterial Swarming
Under sublethal antibiotics concentrations, the statistics of collectively swarming Bacillus subtilis transitions from normal to anomalous, with a heavy-tailed speed distribution and a two-step temporal correlation of velocities. The transition is due to changes in the properties of the bacterial motion and the formation of a motility-defective subpopulation that self-segregates into regions. As a result, both the colonial expansion and the growth rate are not affected by antibiotics. This phenomenon suggests a new strategy bacteria employ to fight antibiotic stress.
Collective motion of spherical bacteria
A large variety of motile bacterial species exhibit collective motions while inhabiting liquids or colonizing surfaces. These collective motions are often characterized by coherent dynamic clusters, where hundreds of cells move in correlated whirls and jets. Previously, all species that were known to form such motion had a rod-shaped structure, which enhances the order through steric and hydrodynamic interactions. Here we show that the spherical motile bacteria Serratia marcescens exhibit robust collective dynamics and correlated coherent motion while grown in suspensions. As cells migrate to the upper surface of a drop, they form a monolayer, and move collectively in whirls and jets. At all concentrations, the distribution of the bacterial speed was approximately Rayleigh with an average that depends on concentration in a non-monotonic way. Other dynamical parameters such as vorticity and correlation functions are also analyzed and compared to rod-shaped bacteria from the same strain. Our results demonstrate that self-propelled spherical objects do form complex ordered collective motion. This opens a door for a new perspective on the role of cell aspect ratio and alignment of cells with regards to collective motion in nature.
Some on the dynamics of marine bacteria
Trichodesmium spp. are diazotrophic cyanobacteria that exist as single filaments (trichomes) and as macroscopic colonies of varying shapes formed by aggregating trichomes. The causes and dynamics of colony formation and disassociation are not yet elucidated. We demonstrate that limited availability of dissolved phosphorus (P) or iron (Fe) stimulated trichome mobility and induced colony formation in Trichodesmium erythraeum IMS101 cultures. The specific nutrient limitation differentially affected the rate of colony formation and morphology of the colonies. Fe starvation promoted rapid colony formation (10–48 h from depletion) while 5–7 days were required for colonies to form in P-depleted cultures. Video analyses confirmed that the probability of trichomes to cluster increased from 12 to 35% when transferred from nutrient replete to Fe depleted conditions. Moreover, the probability for Fe-depleted aggregates to remain colonial increased to 50% from only 10% in nutrient replete cultures. These colonies were also characterized by stronger attachment forces between the trichomes. Enrichment of nutrient-depleted cultures with the limited nutrient-stimulated colony dissociation into single trichomes. We postulate that limited P and Fe availability enhance colony formation of Trichodesmium and primarily control the abundance and distribution of its different morphologies in the nutrient-limited surface ocean.
Competition between colonies
Bacteria can secrete a wide array of antibacterial compounds when competing with other bacteria for the same resources. Some of these compounds, such as bacteriocins, can affect bacteria of similar or closely related strains. In some cases, these secretions have been found to kill sibling cells that belong to the same colony. Here, we present experimental observations of competition between 2 sibling colonies of Paenibacillus dendritiformis grown on a low-nutrient agar gel. We find that neighboring colonies (growing from droplet inoculation) mutually inhibit growth through secretions that become lethal if the level exceeds a well-defined threshold. In contrast, within a single colony developing from a droplet inoculation, no growth inhibition is observed. However, growth inhibition and cell death are observed if material extracted from the agar between 2 growing colonies is introduced outside a growing single colony. To interpret the observations, we devised a simple mathematical model for the secretion of an antibacterial compound. Simulations of this model illustrate how secretions from neighboring colonies can be deadly, whereas secretions from a single colony growing from a droplet are not.
Collective dynamics of long bacteria
Bacterial swarming is a type of motility characterized by a rapid and collective migration of bacteria on surfaces. Most swarming species form densely packed dynamic clusters in the form of whirls and jets, in which hundreds of rod-shaped rigid cells move in circular and straight patterns, respectively. Recent studies have suggested that short-range steric interactions may dominate hydrodynamic interactions and that geometrical factors, such as a cell’s aspect ratio, play an important role in bacterial swarming. Typically, the aspect ratio for most swarming species is only up to 5, and a detailed understanding of the role of much larger aspect ratios remains an open challenge. Here we study the dynamics of Paenibacillus dendritiformis C morphotype, a very long, hyperflagellated, straight (rigid), rod-shaped bacterium with an aspect ratio of20. We find that instead of swarming in whirls and jets as observed in most species, including the shorter T morphotype of P. dendritiformis, the C morphotype moves in densely packed straight but thin long lines. Within these lines, all bacteria show periodic reversals, with a typical reversal time of 20 s, which is independent of their neighbors, the initial nutrient level, agar rigidity, surfactant addition, humidity level, temperature, nutrient chemotaxis, oxygen level, illumination intensity or gradient, and cell length. The evolutionary advantage of this unique back-and-forth surface translocation remains unclear.
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