Surface tension gradient control of bacterial swarming in colonies of Pseudomonas aeruginosa

Abstract

Bacterial swarming is one of the most efficient methods by which bacteria colonize nutrient-rich environments and host tissues. Several mechanisms have been proposed to explain the phenomenon and the associated intricate macroscopic pattern formation, but so far no conclusive evidence has been presented that identifies the factors that control swarming. Vice versa, little is known about how swarming can be controlled. Here, by using a series of complementary genetic and physicochemical experiments and a simple mathematical analysis, we show how the bacterial swarming can be caused by a surface tension driven flow. The opportunistic pathogen, Pseudomonas aeruginosa, is studied, as it is relevant for such bacteria to control and arrest swarming. Moreover, P. aeruginosa bacteria secrete strong surface active components as part of their quorum sensing system. Our results demonstrate that surface tension gradient control can even be the dominant mechanism that drives swarming. It can be quantitatively predicted and can be expected to play a role in a wide variety of bacterial systems. The modeling reveals subtle dependencies on both the wetting conditions and the physical properties of the slime. Based on these dependencies, strategies can be devised to arrest swarming under certain conditions by simple physicochemical means.

Auto-production of biosurfactants reverses the coffee ring effect in a bacterial system

“…Our experiments indicate that biosurfactants have a significant role in the distribution of bacterial systems during drying, in general, in addition to the recently discovered role of self-produced surfactants in transport and movement processes12353637. Although our experiments were only conducted on P. aeruginosa , our conclusions are likely to be widely applicable and there are several other bacteria, which produce strong biosurfactants3538.…”

“…However, P. aeruginosa is not an ideal system to investigate these dynamics using confocal microscopy in detail due to its pathogenic nature and due to the high bacterial density under swarming conditions, which leads to a difficulty in imaging12. Additionally, to have more control over the surfactant type and its concentration in the droplet, non-biosurfactant producing E. coli was used to enable the systematic (more quantitative) study on the influence of exogeneously added surfactant, complementary to the rhamnolipid producing P. aeruginosa .…”

“…P. aeruginosa PA14 wild-type and its rhamnolipid production knock-out mutant were cultivated for swarming experiments according to the protocols in Fauvart et al 12. Conditions for swarming were obtained by inoculating a spot of 2 μl of a P. aeruginosa culture, grown overnight in trypticase soy broth at 37 °C onto plates containing swarming medium (0.5% agar, 0.2% glucose, 1 mM MgSO 4 , 0.05 g casamino acids, 3.4 g Na 2 HPO 4 .…”

The ecological basis of morphogenesis: branching patterns in swarming colonies of bacteria

“…These time-scales may be necessary to describe complex temporal patterns such as high-density waves observed recently in P. aeruginosa colonies using multispectral imaging (Du et al, 2012). Other biophysical process that are not explicitly modeled here but that are known to play important roles in swarming include quorum sensing and metabolic prudence which control rhamnolipid production (Xavier et al, 2011), surface tension (Fauvart et al, 2012; Du et al, 2011), spreading of liquid at the edge of a swarm (Tremblay et al, 2007) and flagellated motion of bacteria in liquid (Kohler et al, 2000; Du et al, 2011; van Ditmarsch et al, 2013). …”

Spreading of nonmotile bacteria on a hard agar plate: Comparison between agent-based and stochastic simulations

“…Bacteria in a Petri dish environment exhibit a large variety of complex spatial patterns ranging from compact circular growth, concentric rings to long branched patterns [4][5][6][7][8][9][10][11]. The colony morphology depends upon various factors such as nutrient concentration, cell motility, growth-proliferation and death dynamics, and other chemical and physical variables [12][13][14][15][16][17][18][19][20]. In a classic experiment, Wakita et al [4] obtained the phase-diagram of Bacillus subtilis colony morphology as a function of nutrient concentration and solidity of agar medium and identified five basic morphologies: (A) diffusion limited aggregation (DLA), (B) Eden-like, (C) concentric ring-like, (D) homogeneous spreading, and (E) dense branching morphology (DBM).…”