Confinement discerns swarmers from planktonic bacteria

Abstract

Powered by flagella, many bacterial species exhibit collective motion on a solid surface commonly known as swarming. As a natural example of active matter, swarming is also an essential biological phenotype associated with virulence, chemotaxis, and host pathogenesis. Physical changes like cell elongation and hyper flagellation have been shown to accompany the swarming phenotype. Less studied, however, are the contrasts of collective motion between the swarming cells and their counterpart planktonic cells of comparable cell density. Here, we show that confining bacterial movement in circular microwells allows distinguishing bacterial swarming from collective swimming. On a soft agar plate, a novel bacterial strain Enterobacter sp. SM3 in swarming and planktonic states exhibited different motion patterns when confined to circular microwells of a specific range of sizes. When the confinement diameter was between 40 μm and 90 μm, swarming SM3 formed a single swirl motion pattern in the microwells whereas planktonic SM3 formed multiple swirls. Similar differential behavior is observed across several other species of gram-negative bacteria. We also observed 'rafting behavior' of swarming bacteria upon dilution. We hypothesize that the rafting behavior might account for the motion pattern difference. We were able to predict these experimental features via numerical simulations where swarming cells are modeled with stronger cell-cell alignment interaction. Our experimental design using PDMS microchip disk arrays enabled us to observe bacterial swarming on murine intestinal surface suggesting a new method for characterizing bacterial swarming under complex environments, such as in polymicrobial niches, and for in vivo swarming exploration.

Multi-population dissolution in confined active fluids

“…These boundaries may be hard walls or soft interfaces and lead to strong effects on the collective motion, patterns, and structure formation in these systems. Chen et al , 36 studied Enterobacter swarms confined in microwells and found that self-organized flows comprising a single vortex for small wells and multiple, smaller vortices for larger wells. In previous work, we have demonstrated that swarms of Serratia marcescens propagating on wet agar also show similar patterns, 26 suggesting that these spatiotemporal features are species-independent features.…”

“…19,20 Equally important are the synergistic effects of motility (selfpropulsion at the single cell level), direct cell-cell interactions that include steric and other biophysical or biochemical interactions, and fluid-mechanical inter-cell interactions mediated by the ambient medium. Combined with boundary interactions and confinement, all these can lead to emergent stable spatiotemporal patterns and transitions between states that are structurally distinct; examples of these are swimming-toswarming transitions demonstrated recently in bacteria confined to wells, 36 spatiotemporally fluctuating arrayed vortices, 26 and activitydependent jamming in growing bacterial colonies. [37][38][39] Motilitydriven mixing may also result in domain formation, creating interfaces [21][22][23][24] that may fragment, propagate or mix.…”

“…47 Agent-based models without full hydrodynamics (typically called dry simulations) were also utilized to study confined single-species swarming bacteria. 36,48 The second approach focuses on solving mean-field mesoscale continuum kinetic models with coarse-grained interactions. The resulting model may correspond to dry systems without hydrodynamic interactions 48,50 or wet systems with hydrodynamic interactions that include a description of the underlying fluid motion.…”

Multi-population dissolution in confined active fluids

“…Equally important are the synergistic effects of motility (self-propulsion at the single cell level), direct cell-cell interactions that include steric and other biophysical or biochemical interactions, and fluid-mechanical intercell interactions mediated by the ambient medium. Combined with boundary interactions and confinement, all these can lead to emergent stable spatiotemporal patterns and transitions be-tween states that are structurally distinct; examples of these are swimming-to-swarming transitions demonstrated recently in bacteria confined to wells 36 , spatiotemporally fluctuating arrayed vortices 26 , and activity-dependent jamming in growing bacterial colonies [37][38][39] . Motility-driven mixing may also result in domain formation, creating interfaces [21][22][23][24] that may fragment, propagate or mix 26,27,40 .…”

“…Such discrete agent-based simulations have been used to study microswimmer suspensions [41][42][43][44][45][46] , and active nematic liquid crystalline phases 47 . Agent-based models without full hydrodynamics (typically called dry simulations) were also utilized to study confined singlespecies swarming bacteria 36,48 . The second approach focuses on solving mean-field mesoscale continuum kinetic models with coarse-grained interactions.…”