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

Abstract

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.I n the wide variety of systems termed "active matter" (1, 2), one finds the spontaneous appearance of coherent dynamic structures on scales that are large compared with the individual motile units. Examples range from polar gels (3, 4), bacterial suspensions (5-10), and microtubule bundles (11) to cytoplasmic streaming (12, 13). At high concentrations, suspensions of rodlike bacteria are known to arrange at the cellular scale with parallel alignment as in nematic liquid crystals (5, 14), but with local order that is polar, driven by motility (15, 16). At meso-and macroscopic scales, coherent structures such as swirls, jets, and vortices at scales 10 μm to 1 mm have been experimentally observed (5-10). Many studies have focused on how complex cell interactions can give rise to macroscopic organization and ordering, and the role of self-generated fluid flows in the dynamics of dense suspensions is still under debate (8,10,(17)(18)(19)(20)(21). This controversy is due in part to the inherent complexity of the systems under investigation and the difficulty in making faithful mathematical models.Microswimmers such as Escherichia coli, Bacillus subtilis, and Chlamydomonas rheinhardtii produce dipolar fluid flows through the combined action of their flagella and cell body on the fluid. In the far field, they are well described as "pusher" or "puller" stresslets (22-24), corresponding to the case of f...

Geometry-dependent viscosity reduction in sheared active fluids

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Batchelor Prize Lecture Fluid dynamics at the scale of the cell

“…In addition to the predicted global behaviour, this experiment had a surprising and unanticipated feature: a counter-rotating boundary layer at the drop periphery ('edge current'), perhaps one or two cells wide. It was initially unclear the direction in which the cells were swimming in this layer, relative to the bulk, but numerical studies (Lushi, Wioland & Goldstein 2014) suggested the counterintuitive result that the cells within the bulk vortex actually swim upstream against the 'backwash' from the boundary layer. This prediction was verified by use of a two-colour fluorescent labelling technique that allows one to visualise the cell body separately from the flagella, and thereby arrive at an unambiguous determination of the cell orientations in the domain.…”

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