Concentrated suspensions of swimming microorganisms and other forms of active matter are known to display complex, self-organized spatiotemporal patterns on scales that are large compared with those of the individual motile units. Despite intensive experimental and theoretical study, it has remained unclear the extent to which the hydrodynamic flows generated by swimming cells, rather than purely steric interactions between them, drive the self-organization. Here we use the recent discovery of a spiral-vortex state in confined suspensions of Bacillus subtilis to study this issue in detail. Those experiments showed that if the radius of confinement in a thin cylindrical chamber is below a critical value, the suspension will spontaneously form a steady single-vortex state encircled by a counter-rotating cell boundary layer, with spiral cell orientation within the vortex. Left unclear, however, was the flagellar orientation, and hence the cell swimming direction, within the spiral vortex. Here, using a fast simulation method that captures oriented cell–cell and cell–fluid interactions in a minimal model of discrete particle systems, we predict the striking, counterintuitive result that in the presence of collectively generated fluid motion, the cells within the spiral vortex actually swim upstream against those flows. This prediction is then confirmed by the experiments reported here, which include measurements of flagella bundle orientation and cell tracking in the self-organized state. These results highlight the complex interplay between cell orientation and hydrodynamic flows in concentrated suspensions of microorganisms.

https://absimage.aps.org/image/MAR16/MWS_MAR16-2015-005717.pdf

Fluid flows created by swimming bacteria drive self-organization in confined suspensions

An analytic model now provides quantitative predictions for the effect of void fractions within a granular medium on avalanche statistics. It will help us understand the dynamics of earthquakes as well as plasticity. Slowly sheared granular materials at high packing fractions deform via slip avalanches with a broad range of sizes. Conventional continuum descriptions1 are not expected to apply to such highly inhomogeneous, intermittent deformations. Here, we show that it is possible to analytically compute the dynamics using a simple model that is inherently discrete. This model predicts quantities such as the avalanche size distribution, power spectra and temporal avalanche profiles as functions of the grain number fraction v and the frictional weakening ɛ. A dynamical phase diagram emerges with quasi-static avalanches at high number fractions, and more regular, fluid-like flow at lower number fractions. The predictions agree with experiments and simulations for different granular materials, motivate future experiments and provide a fresh approach to data analysis. The simplicity of the model reveals quantitative connections to plasticity and earthquake statistics.

http://absimage.aps.org/image/MAR12/MWS_MAR12-2011-002498.pdf

A simple analytic theory for the statistics of avalanches in sheared granular materials

Bacteria have developed a large array of motility mechanisms to exploit available resources and environments. These mechanisms can be broadly classified into swimming in aqueous media and movement over solid surfaces. Swimming motility involves either the rotation of rigid helical filaments through the external medium or gyration of the cell body in response to the rotation of internal filaments. On surfaces, bacteria swarm collectively in a thin layer of fluid powered by the rotation of rigid helical filaments, they twitch by assembling and disassembling type IV pili, they glide by driving adhesins along tracks fixed to the cell surface and, finally, non-motile cells slide over surfaces in response to outward forces due to colony growth. Recent technological advances, especially in cryo-electron microscopy, have greatly improved our knowledge of the molecular machinery that powers the various forms of bacterial motility. In this Review, we describe the current understanding of the physical and molecular mechanisms that allow bacteria to move around.

Bacterial motility: machinery and mechanisms.

Superhydrophobic surfaces are promising for preventing fouling and the formation of biofilms, with important implications in the food chain, maritime transport, and health sciences, among others. In this work, we exploit the interplay between wetting principles of superhydrophobic surfaces and microbial fouling for advanced three-dimensional (3D) biofabrication of biofilms. We utilize hydrostatic and capillary pressures to finely control the air-water interface and the aerotaxis-driven biofabrication on superhydrophobic surfaces. Superhydrophobic 3D molds are produced by a simple surface modification that partially embeds hydrophobic particles in silicone rubber. Thereafter, the molds allow the templating of the air-water interface of the culture medium, where the aerobic nanocellulose-producing bacteria (Komagataeibacter medellinensis) are incubated. The biofabricated replicas are hollow and seamless nanofibrous objects with a controlled morphology. Gradients of thickness, topographical feature size, and fiber orientation on the biofilm are obtained by controlling wetting, incubation time, and nutrient availability. Furthermore, we demonstrate that capillary length limitations are overcome by using pressurized closed molds, whereby a persistent air plastron allows the formation of 3D microstructures, regardless of their morphological complexity. We also demonstrate that interfacial biofabrication is maintained for at least 12 days without observable fouling of the mold surface. In summary, we achieve controlled biofouling of the air-water interface as imposed by the experimental framework under controlled wetting. The latter is central to both microorganism-based biofabrication and fouling, which are major factors connecting nanoscience, synthetic biology, and microbiology.

/pdf/guiding-bacterial-activity-for-biofabrication-of-complex-3jlfbe705n.pdf

Guiding Bacterial Activity for Biofabrication of Complex Materials via Controlled Wetting of Superhydrophobic Surfaces

Significance How bacteria propagate and colonize new environments is of paramount importance, e.g., to food processing, transport, and storage. In this article, we show that Bacillus subtilis can turn millimetric water droplets into vehicles to quickly cover large distances. To this end, they overcome the enormous capillary forces that prevent the sliding of water droplets even on vertical surfaces such as refrigerator walls. B. subtilis does so by actively unpinning the surrounding liquid to cause the collective surfing of the entire community on slopes as small as 0.1°. We show this depinning to rely on a variety of mechanisms, which could each be relevant to the motility of microorganisms in partially humid environments such as unsaturated soils. How systems are endowed with migration capacity is a fascinating question with implications ranging from the design of novel active systems to the control of microbial populations. Bacteria, which can be found in a variety of environments, have developed among the richest set of locomotion mechanisms both at the microscopic and collective levels. Here, we uncover, experimentally, a mode of collective bacterial motility in humid environment through the depinning of bacterial droplets. Although capillary forces are notoriously enormous at the bacterial scale, even capable of pinning water droplets of millimetric size on inclined surfaces, we show that bacteria are able to harness a variety of mechanisms to unpin contact lines, hence inducing a collective slipping of the colony across the surface. Contrary to flagella-dependent migration modes like swarming, we show that this much faster “colony surfing” still occurs in mutant strains of Bacillus subtilis lacking flagella. The active unpinning seen in our experiments relies on a variety of microscopic mechanisms, which could each play an important role in the migration of microorganisms in humid environment.

/pdf/active-depinning-of-bacterial-droplets-the-collective-b34csazmct.pdf

Active depinning of bacterial droplets: the collective surfing of Bacillus subtilis

Microbes routinely face the challenge of acquiring territory and resources on wet surfaces Cells move in large groups inside thin, surface-bound water layers, often achieving speeds of 30 µm s-1 within this environment, where viscous forces dominate over inertial forces (low Reynolds number) The canonical Gram-positive bacterium Bacillus subtilis is a model organism for the study of collective migration over surfaces with groups exhibiting motility on length-scales three orders of magnitude larger than themselves within a few doubling times Genetic and chemical studies clearly show that the secretion of endogenous surfactants and availability of free surface water are required for this fast group motility Here, we show that: (i) water availability is a sensitive control parameter modulating an abiotic jamming-like transition that determines whether the group remains fluidized and therefore collectively motile, (ii) groups self-organize into discrete layers as they travel, (iii) group motility does not require proliferation, rather groups are pulled from the front, and (iv) flow within expanding groups is capable of moving material from the parent colony into the expanding tip of a cellular dendrite with implications for expansion into regions of varying nutrient content Together, these findings illuminate the physical structure of surface-motile groups and demonstrate that physical properties, like cellular packing fraction and flow, regulate motion from the scale of individual cells up to length scales of centimetres

https://royalsocietypublishing.org/doi/pdf/10.1098/rsif.2020.0147

Bacterial surface motility is modulated by colony-scale flow and granular jamming.

Microbes routinely face the challenge of acquiring territory and resources on wet surfaces. Cells move in large groups inside thin, surface-bound water layers, often achieving speeds of 30 μm/s within this environment, where viscous forces dominate over inertial forces (low Reynolds number). The canonical Gram-positive bacterium Bacillus subtilis is a model organism for the study of collective migration over surfaces with groups exhibiting motility on length scales three orders of magnitude larger than themselves within a few doubling times. Genetic and chemical studies clearly show that the secretion of endogenous surfactants and availability of free surface water are required for this fast group motility. Here we show that: (i) water availability is a sensitive control parameter modulating an abiotic jamming-like transition that determines whether the group remains fluidized and therefore collectively motile, (ii) groups self-organize into discrete layers as they travel, (iii) group motility does not require proliferation, rather groups are pulled from the front, and (iv) flow within expanding groups is capable of moving material from the parent colony into the expanding tip of a cellular dendrite with implications for expansion into regions of varying nutrient content. Together, these findings illuminate the physical structure of surface-motile groups and demonstrate that physical properties, like cellular packing fraction and flow, regulate motion from the scale of individual cells up to length scales of centimeters.

/pdf/physical-factors-contributing-to-regulation-of-bacterial-my5fvfapan.pdf

Physical factors contributing to regulation of bacterial surface motility

In their search for metabolic resources microbes swim through viscous environments that present physical anisotropies, including steric obstacles across a wide range of sizes. Hydrodynamic forces are known to significantly alter swimmer trajectories near flat and low-curvature surfaces. In this work, we imaged hundreds-of-thousands of high-curvature scattering interactions between swimming bacteria and micro-fabricated pillars with radii from ~1 to ~10 cell lengths. As a function of impact parameter, cell-pillar interactions produced distinct chiral distributions for scattering angle -- including unexpected 'counter-rotator' trajectories -- well-described by a sterics-only model. Our data and model suggest that alteration of swimmer trajectories is subject to distinct mechanisms when interacting with objects of different size; primarily steric for objects below ~10 cell lengths and requiring incorporation of hydrodynamics at larger scales. These alterations in trajectory impact swim dynamics and may affect microbial populations in ways that depend on the shape and placement of obstacles within an environment.

Scattering of rod-like swimmers in low Reynolds number environments

Microbes form integral components of all natural ecosystems. In most cases, the surrounding micro-environment has physical variations that affect the movements of micro-swimmers, including solid objects of varying size, shape and density. As swimmers move through viscous environments, a combination of hydrodynamic and steric forces are known to significantly alter their trajectories in a way that depends on surface curvature. In this work, our goal was to clarify the role of steric forces when rod-like swimmers interact with solid objects comparable to cell size. We imaged hundreds-of-thousands of scattering interactions between swimming bacteria and micro-fabricated pillars with radii from ∼1 to ∼10 cell lengths. Scattering interactions were parameterized by the angle of the cell upon contact with the pillar, and primarily produced forward-scattering events that fell into distinct chiral distributions for scattering angle – no hydrodynamic trapping was observed. The chirality of a scattering event was a stochastic variable whose probability smoothly and symmetrically depended on the contact angle. Neglecting hydrodynamics, we developed a model that only considers contact forces and torques for a rear-pushed thin-rod scattering from a cylinder – the model predictions were in good agreement with measured data. Our results suggest that alteration of bacterial trajectories is subject to distinct mechanisms when interacting with objects of different size; primarily steric for objects below ∼10 cell lengths and requiring incorporation of hydrodynamics at larger scales. These results contribute to a mechanistic framework in which to examine (and potentially engineer) microbial movements through natural and synthetic environments that present complex steric structure.

Kentaro Hoeger

Papers

Bacterial surface motility is modulated by colony-scale flow and granular jamming.

Physical factors contributing to regulation of bacterial surface motility

Scattering of rod-like swimmers in low Reynolds number environments

Steric scattering of rod-like swimmers in low Reynolds number environments.