Noncontact Cohesive Swimming of Bacteria in Two-Dimensional Liquid Films

Ye Li, He Zhai, Sandra Sanchez, Daniel B. Kearns, and Yilin Wu

Phys. Rev. Lett. 119, 018101 – Published 5 July 2017

Abstract

Bacterial swimming in confined two-dimensional environments is ubiquitous in nature and in clinical settings. Characterizing individual interactions between swimming bacteria in 2D confinement will help to understand diverse microbial processes, such as bacterial swarming and biofilm formation. Here we report a novel motion pattern displayed by flagellated bacteria in 2D confinement: When two nearby cells align their moving directions, they tend to engage in cohesive swimming without direct cell body contact, as a result of hydrodynamic interaction but not flagellar intertwining. We further found that cells in cohesive swimming move with higher directional persistence, which can increase the effective diffusivity of cells by $\sim 3$ times as predicted by computational modeling. As a conserved behavior for peritrichously flagellated bacteria, cohesive swimming in 2D confinement may be key to collective motion and self-organization in bacterial swarms; it may also promote bacterial dispersal in unsaturated soils and in interstitial space during infections.

Received 4 October 2016

DOI:https://doi.org/10.1103/PhysRevLett.119.018101

Physics Subject Headings (PhySH)

Biological self-organization Cell locomotion Collective behavior Swarming

Biofilms Low Reynolds number swimmers

Physics of Living SystemsInterdisciplinary PhysicsFluid Dynamics

Authors & Affiliations

Ye Li¹, He Zhai², Sandra Sanchez³, Daniel B. Kearns³, and Yilin Wu^1,*

¹Department of Physics and Shenzhen Research Institute, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, People’s Republic of China
²Northwest Institute For Nonferrous Metal Research, 96 Weiyang Street, Xian, Shaanxi 710016, People’s Republic of China
³Department of Biology, Indiana University, 1001 East 3rd Street, Bloomington, Indiana 47405, USA

^*To whom correspondence should be addressed. ylwu@phy.cuhk.edu.hk

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Vol. 119, Iss. 1 — 7 July 2017

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Images

Figure 1
Noncontact cohesive swimming of bacteria. (a) Two wildtype B. subtilis cells approached each other and swam cohesively for $\sim 3.7 s$ without direct cell body contact. Dashed lines represent trajectories of the two cells. Scale bar, $20 μ m$ . Also see Supplemental Material, movie 1 [42]. (b) An image sequence of the zoomed-in view of the cell pair undergoing cohesive swimming in panel (a). The centers of the cell pair are labeled by white and red dots. Scale bar, $5 μ m$ . (c) Nearest distance between the two cells in panel (a) plotted against time. The shaded area indicates the duration of cohesive swimming. The nearest distance is zero if two cells are in direct body contact.
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Figure 2
Probability distribution of trapping time for cohesively swimming cell pairs of B. subtilis. (a) Wildtype, (b) smooth-swimming mutant, bin size is 0.6 s. The trapping time is defined as the time duration traveled by two cohesively swimming cells before they separate spontaneously. Two cells are considered as engaging in cohesive swimming if the distance between their centers is less than their average length and if the angle between their velocity directions is less than 10º. The mean trapping time of wildtype and smooth-swimming B. subtilis is $1.10 \pm 0.55 s$ ( $mean \pm s . d .$ , $n = 94$ ) and $1.55 \pm 0.95 s$ ( $mean \pm SD$ , $n = 82$ ), respectively.
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Figure 3
Flagellar dynamics of two cells undergoing noncontact cohesive swimming. Flagellar filaments of B. subtilis DK2178 cells were fluorescently labeled and appeared bright in the image sequence. The two black arrows indicate the orientations of two cells that approached each other and traveled as a cohesive pair. Scale bar, $10 μ m$ . See Supplemental Material, movie 6 [42].
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Figure 4
(a) Auto correlation of cells’ velocity direction measured in experiments. Red circles correspond to cells moving as cohesive pairs ( $n = 126$ cells), and black circles correspond to individually moving cells ( $n = 96$ cells). Bars represent standard error of the mean. (b) Illustration of 4 possible scenarios of cell-wall interaction for a pair of cells undergoing cohesive swimming. Cells colored in pink (or blue) interact with the upper (or lower) wall and tend to curve to the left (or to the right). The two cells in scenarios (iii) and (iv) interact with opposite walls, so the pair has reduced directional bias. (c) Spatial distribution of modeled cells with (left) and without (right) the ability to engage in cohesive swimming at the end of a typical simulation run. Red dots represent cells undergoing cohesive swimming and black dots represent cells moving individually. Note that a given cell alternates between the red and black state, with the frequency of the red state depending on collision rate (or local cell density), so at any specific time most cells in the red state are located in the inner region where cell density is higher. The duration of the simulation corresponds to cell dispersal for 1000 s. Scale bar, 5 mm. See Supplemental Material, movie 7 [42]. (d) Mean square displacement (MSD) of cells in simulations shown in (c). Red and black lines plot the average MSD ( $n = 5$ independent simulation runs) for populations with and without the ability to engage in cohesive swimming, respectively.
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