Antibiotic-Induced Anomalous Statistics of Collective Bacterial Swarming

Sivan Benisty, Eshel Ben-Jacob, Gil Ariel, and Avraham Be’er

Phys. Rev. Lett. 114, 018105 – Published 6 January 2015

Abstract

Under sublethal antibiotics concentrations, the statistics of collectively swarming Bacillus subtilis transitions from normal to anomalous, with a heavy-tailed speed distribution and a two-step temporal correlation of velocities. The transition is due to changes in the properties of the bacterial motion and the formation of a motility-defective subpopulation that self-segregates into regions. As a result, both the colonial expansion and the growth rate are not affected by antibiotics. This phenomenon suggests a new strategy bacteria employ to fight antibiotic stress.

Received 7 August 2014

DOI:https://doi.org/10.1103/PhysRevLett.114.018105

Authors & Affiliations

Sivan Benisty¹, Eshel Ben-Jacob^2,3, Gil Ariel⁴, and Avraham Be’er^1,*

¹Zuckerberg Institute for Water Research, The Jacob Blaustein Institutes for Desert Research, Ben-Gurion University of the Negev, Sede Boqer Campus 84990, Midreshet Ben-Gurion, Israel
²School of Physics and Astronomy, Raymond and Beverly Sackler Faculty of Exact Sciences, Tel Aviv University, Tel Aviv 69978, Israel
³Center for Theoretical Biological Physics, Rice University, Houston, Texas 77025, USA
⁴Department of Mathematics, Bar-Ilan University, Ramat Gan 52000, Israel

^*Corresponding author. beera@bgu.ac.il

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Vol. 114, Iss. 1 — 9 January 2015

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Images

Figure 1
B. subtilis swarming colonies. Left: Top-view phase contrast microscopic image of a swarm taken close to the colony’s edge. Red lines separate regions of very slowly moving cells (static clusters) from fast moving cells. (a) No added antibiotics. Regions encircled by red are stationary. (c) With added $0.08 μ g / ml$ kanamycin. Regions encircled by red are moving. Right: The instantaneous velocity field at the same time. Colors indicate clockwise (red) or counterclockwise (blue) motion. (b) No added antibiotics and (d) with added $0.08 μ g / ml$ kanamycin. The scale bar is $10 μ m$ .
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Figure 2
The effects of kanamycin. (a) Number of CFU (live bacteria) at the colony edge using three different measurement methods (red, blue, and green) and the average expansion rate of the colony (black), indicating that the colony’s expansion is not affected. (b) The average speed of the swarm gradually decreases with added kanamycin. (c) The centered distribution of the $x$ and $y$ components of the velocity. The 0 kanamycin curve is Gaussian. (d) The scaled fourth moment (kurtosis) of the velocity distribution functions changes from 3 (Gaussian) for antibiotic-free samples to 6 (exponential tail) and even larger at high concentrations.
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Figure 3
A double exponential decay in the directional correlation function $\hat{C} (t)$ . (a) A close to exponential decay for the 0 kanamycin case (black curve). A double exponential decay for the $0.08 μ g / ml$ kanamycin case (gray curve). The two time scales weakly depend on the antibiotic concentration (Fig. S2). (b) The contribution (amplitudes) of each exponent as a function of kanamycin. The relative contribution of each time scale switches from mostly slow to mostly fast at around $0.075 μ g / ml$ kanamycin.
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Figure 4
Experimental (dots) and simulation (lines) results for mixtures of motile and immotile cells. (a) The mean speed, (b) the kurtosis of the velocity distribution, and (c) amplitudes of the double exponential decay in the directional correlation function $\hat{C} (t)$ . Compare with the antibiotic treated experiments Figs. 2, 2, and 3. (d) The fraction of motile and immotile particles taking part of the clusters as a function of permutation rate. Points on the $y$ axis indicate the no-permutation case. At high rates, motile and immotile particles behave similarly. However, at sufficiently low rates the system self-segregates into immotile clusters and with motile particles moving between them.
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