Microbubbles reveal chiral fluid flows in bacterial swarms

ArticleinProceedings of the National Academy of Sciences 108(10):4147-51 · February 2011with51 Reads
DOI: 10.1073/pnas.1016693108 · Source: PubMed
Abstract
Flagellated bacteria can swim within a thin film of fluid that coats a solid surface, such as agar; this is a means for colony expansion known as swarming. We found that micrometer-sized bubbles make excellent tracers for the motion of this fluid. The microbubbles form explosively when small aliquots of an aqueous suspension of droplets of a water-insoluble surfactant (Span 83) are placed on the agar ahead of a swarm, as the water is absorbed by the agar and the droplets are exposed to air. Using these bubbles, we discovered an extensive stream (or river) of swarm fluid flowing clockwise along the leading edge of an Escherichia coli swarm, at speeds of order 10 μm/s, about three times faster than the swarm expansion. The flow is generated by the action of counterclockwise rotating flagella of cells stuck to the substratum, which drives fluid clockwise around isolated cells (when viewed from above), counterclockwise between cells in dilute arrays, and clockwise in front of cells at the swarm edge. The river provides an avenue for long-range communication in the swarming colony, ideally suited for secretory vesicles that diffuse poorly. These findings broaden our understanding of swarming dynamics and have implications for the engineering of bacterial-driven microfluidic devices.
    • "The biological hypothesis that the observed chiral flow is driven by the flagella sticking out of the swarm is fully consistent with the predictions of our model. We predict that the flagella are not wrapped around the cells, in contrast to what was found for sparse distributions of bacteria above the agar-creating circulations around the individual cells [22] and for stuck cells [28]. According to our results, the flagella are pointing almost radially out of the swarm contributing to the fluid movement in the radial direction due to pushing on the fluid and creating the chiral flow in the clockwise direction due to the torque applied to the fluid. "
    [Show abstract] [Hide abstract] ABSTRACT: Flagellated bacteria on nutrient-rich substrates can differentiate into a swarming state and move in dense swarms across surfaces. A recent experiment measured the flow in the fluid around an Escherichia coli swarm (Wu, Hosu and Berg, 2011 Proc. Natl. Acad. Sci. USA 108 4147). A systematic chiral flow was observed in the clockwise direction (when viewed from above) ahead of the swarm with flow speeds of about 10 µm/s, about 3 times greater than the radial velocity at the edge of the swarm. The working hypothesis is that this flow is due to the action of cells stalled at the edge of a colony which extend their flagellar filaments outwards, moving fluid over the virgin agar. In this work we quantitatively test his hypothesis. We first build an analytical model of the flow induced by a single flagellum in a thin film and then use the model, and its extension to multiple flagella, to compare with experimental measurements. The results we obtain are in agreement with the flagellar hypothesis. The model provides further quantitative insight on the flagella orientations and their spatial distributions as well as the tangential speed profile. In particular, the model suggests that flagella are on average pointing radially out of the swarm and are not wrapped tangentially.
    Article · Jul 2016 · Frontiers in Microbiology
    • "Cells interact strongly with the swarm fluid film: the fluidic environment supports flagellar motility, while flagellar rotation strongly agitates the swarm fluid and generates rapid flows with speeds up to tens of micron per second [51,63]. Fluid flows driven by flagellar motility can facilitate material transport, promote social interactions, and affect the collective motion in swarms [51] (Chen C., Liu S., Wu Y., unpublished data). "
    [Show abstract] [Hide abstract] ABSTRACT: Collective motion can be observed in biological systems over a wide range of length scales, from large animals to bacteria. Collective motion is thought to confer an advantage for defense and adaptation. A central question in the study of biological collective motion is how the traits of individuals give rise to the emergent behavior at population level. This question is relevant to the dynamics of general self-propelled particle systems, biological self-organization, and active fluids. Bacteria provide a tractable system to address this question, because bacteria are simple and their behavior is relatively easy to control. In this mini review we will focus on a special form of bacterial collective motion, i.e., bacterial swarming in two dimensions. We will introduce some organization principles known in bacterial swarming and discuss potential means of controlling its dynamics. The simplicity and controllability of 2D bacterial behavior during swarming would allow experimental examination of theory predictions on general collective motion.
    Article · Dec 2015
    • "In fact, water is commonly observed in swarms formed by gram-negative bacteria, such as Escherichia coli and Salmonella enterica (Chen et al., 2007; Zhang et al., 2010; Wu et al., 2011; Ping et al., 2014). It is known that an E. coli swarm has water extending about 30 µm ahead of the edge of the swarm (Wu and Berg, 2012), and flagellar motion has been shown to induce fluid flows in E. coli swarms, pointing to the presence of substantial amounts of water (Wu et al., 2011). Fluid osmolarity within a swarm remains high, allowing water in the agar to be extracted, and a recent study found that an E. coli swarm has a high-osmolarity region at the edge and a low-osmolarity region within (Ping et al., 2014). "
    [Show abstract] [Hide abstract] ABSTRACT: Many Bacillus subtilis strains swarm, often forming colonies with tendrils on agar medium. It is known that B. subtilis swarming requires flagella and a biosurfactant, surfactin. In this study, we find that water surface tension plays a role in swarming dynamics. B. subtilis colonies were found to contain water, and when a low amount of surfactin is produced, the water surface tension of the colony restricts expansion, causing bacterial density to rise. The increased density induces a quorum sensing response that leads to heightened production of surfactin, which then weakens water surface tension to allow colony expansion. When the barrier formed by water surface tension is breached at a specific location, a stream of bacteria swarms out of the colony to form a tendril. If a B. subtilis strain produces surfactin at levels that can substantially weaken the overall water surface tension of the colony, water floods the agar surface in a thin layer, within which bacteria swarm and migrate rapidly. This study sheds light on the role of water surface tension in regulating B. subtilis swarming, and provides insight into the mechanisms underlying swarming initiation and tendril formation.
    Full-text · Article · Sep 2015
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