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Dynamic Motility Selection Drives Population Segregation in a Bacterial Swarm

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Dynamic Motility Selection Drives Population Segregation in a Bacterial Swarm Dynamic motility selection drives population segregation in a bacterial swarm Wenlong Zuoa,b and Yilin Wu (吴艺林)a,b,1 aDepartment of Physics, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, People’s Republic of China; and bShenzhen Research Institute, The Chinese University of Hong Kong, Shenzhen 518057, People’s Republic of China Edited by E. Peter Greenberg, University of Washington, Seattle, WA, and approved January 22, 2020 (received for review October 11, 2019) Population expansion in space, or range expansion, is widespread heterogeneity may affect the dynamics of population structure in nature and in clinical settings. Space competition among during range expansion. heterogeneous subpopulations during range expansion is essen- Here we discovered that motility heterogeneity can promote tial to population ecology, and it may involve the interplay of the spatial segregation of subpopulations in structured microbial multiple factors, primarily growth and motility of individuals. communities via a dynamic motility selection mechanism. Our Structured microbial communities provide model systems to study finding was made with swarming bacterial colonies (20–22). By space competition during range expansion. Here we use bacterial tracking single-cell motion pattern and measuring population swarms to investigate how single-cell motility contributes to space structure during swarm expansion, we uncover a linear relation competition among heterogeneous bacterial populations during between single-cell speed and the motion bias toward the swarm range expansion. Our results revealed that motility heterogeneity edge, which presumably arises from physical interactions in the can promote the spatial segregation of subpopulations via a dense swarm. This emergent motion pattern results in a dynamic dynamic motility selection process. The dynamic motility selection motility selection process in dense swarms that causes spatial is enabled by speed-dependent persistence time bias of single-cell segregation of subpopulations with different motilities. We fur- motion, which presumably arises from physical interaction be- ther showed that swarms may employ this dynamic motility se- tween cells in a densely packed swarm. We further showed that lection process to segregate subpopulations with transient drug the dynamic motility selection may contribute to collective drug tolerance to the swarm edge, thereby sustaining colony expansion tolerance of swarming colonies by segregating subpopulations into regions with lethal antibiotic concentrations. with transient drug tolerance to the colony edge. Our results The empirical relation between cell speed and motion bias we BIOPHYSICS AND COMPUTATIONAL BIOLOGY “ ” illustrate that motility heterogeneity, or motility fitness, can uncovered offers a unique mechanism via which individual mo- play a greater role than growth rate fitness in determining the tility may contribute to space competition among heterogeneous short-term spatial structure of expanding populations. microbial populations during range expansion. Like in other organisms, space competition in microbial communities is crucial bacterial swarming | flagellar motility | antibiotic tolerance | adaptive to population survival and interaction. Our findings are therefore stress response | collective motion relevant to microbial stress response and ecology. The findings are also relevant to range expansion in other biological systems, APPLIED PHYSICAL SCIENCES opulation expansion in space (or range expansion) is wide- such as tumor invasion and collective stress tolerance of cancer Pspread in nature and in clinical settings; examples include cells in densely packed environments (2, 23). migration of alien species (1), cancer invasion (2), and microbial dispersal (3, 4). As phenotypic and genetic heterogeneity often Significance exist in populations, space competition among the heteroge- neous subpopulations during range expansion is essential to niche dynamics and to the evolutionary dynamics of genetic Ecological models usually take growth rate fitness as the es- sential driver of population dynamics. However, as a wide- mutations (5, 6). Such space competition may involve the in- spread natural phenomenon, population expansion in space (or terplay of multiple factors, primarily growth and motility (or range expansion) is often governed by both motility and dispersal rate) (7–9). Understanding how growth and motility growth. Microbial communities offer unique systems to study control the dynamics of space competition among subpopula- how an individual’s motility contributes to space competition tions may provide insights on diverse range-expansion processes. among heterogeneous microbial populations during range Structured microbial communities offer tractable model sys- expansion. Here we show that motility heterogeneity can tems to study range expansion (8, 10–13). In particular, with ’ promote the spatial segregation of subpopulations in struc- convenience to manipulate individual cells motility or collective tured microbial communities via a dynamic motility selection dispersal rate, microbial communities are well suited to study the mechanism. Our findings are relevant to microbial stress re- role of motility in space competition among subpopulations. sponse and microbial ecology. The results may also provide Indeed, experiments with engineered microbial communities new insight to range expansion in other biological systems, demonstrated the paradoxical phenomenon that dispersal could such as tumor invasion and collective stress tolerance of cancer reduce population spread [i.e., the Allee effect (14)] (8, 15); cells in densely packed environments. recent studies have revealed important insights on how trade-off between growth and motility controls the long-term dynamics of Author contributions: W.Z. and Y.W. designed research; W.Z. performed research; W.Z. space competition in expanding microbial communities (12, 13). and Y.W. contributed new reagents/analytic tools; W.Z. and Y.W. analyzed data; and Y.W. In these studies the role of motility in space competition was wrote the paper. addressed over long time scales that span many generations, and The authors declare no competing interest. individual motility was often coupled to growth. At shorter time This article is a PNAS Direct Submission. scales before growth selection has taken effect, it is usually Published under the PNAS license. believed that individual cells’ motility promotes population 1To whom correspondence may be addressed. Email: [email protected]. mixing and blurs the boundaries between subpopulations (16, This article contains supporting information online at https://www.pnas.org/lookup/suppl/ 17). However, microbial communities often consist of subpopu- doi:10.1073/pnas.1917789117/-/DCSupplemental. lations with different motilities (18, 19). It is unclear how motility www.pnas.org/cgi/doi/10.1073/pnas.1917789117 PNAS Latest Articles | 1of8 Downloaded by guest on September 26, 2021 Results A Inoculation Incubate high on i Spatial Segregation of Subpopulations with Different Motilities in the c oti trat n Swarm. Mix ibi To investigate the effect of motility heterogeneity on t + e space competition during microbial range expansion, we chose to An cons work with Escherichia coli, a model bacterium displaying robust swarming behavior on agar surfaces. Swarming is a specialized B form of surface translocation exhibited by many flagellated bacterial species (20–22). Cells in a bacterial swarm move ac- tively in quasi-two-dimensional (2D) fluidic environment (24–29) C and they do not perform chemotaxis (30), so swarms provide a unique system to investigate how motility per se affects population -18 -12 -6 0 6 12 18 24 structure during range expansion. As E. coli strains with swarming mm capability but with variable speed are not available, we used an- D tibiotic treatment to artificially induce motility heterogeneity in E. 10 0 coli swarms. Specifically, we subjected E. coli cells to the stress of the aminoglycoside drug kanamycin (KAN) that collaterally re- duces flagellar motility (31–33) (SI Appendix,Fig.S1). We grew E. 10 -1 coli swarms on antibiotic-gradient agar plates; in such an agar All) Ratio (YW 191 / plate, half of the plate was infused with a linear gradient of KAN 10 0 10 20 10 0 10 20 10 0 10 20 − − Distance (mm) (concentration gradient: 12.5 μg∙mL 1∙cm 1) while the other half was left drug-free (Fig. 1A, SI Appendix, Fig. S2,andMethods). A Fig. 1. Spatial segregation of subpopulations with motility heterogeneity mixture of two E. coli populations, one having genetically encoded in E. coli swarms. (A) Illustration of the protocol to induce motility hetero- KAN resistance (labeled by green fluorescent protein, GFP) and geneity in E. coli swarms on an antibiotic gradient plate. E. coli YW191 cells (KAN-resistant, labeled by GFP) and YW263 (KAN-sensitive, labeled by the other sensitive to KAN (labeled by red fluorescent protein, Katushka2S) were mixed and inoculated onto the drug-free side of a KAN Katushka2S), was inoculated onto the drug-free side of such gradient plate (SI Appendix, Fig. S2 and Methods). The dashed line on the gradient plates at an initial population ratio 1:10 (Fig. 1A, SI plate marks the boundary between drug-free and drug-infused regions on Appendix,Fig.S2,andMethods). The two strains have no motility the plate, and the color scale indicates relative KAN concentration. The difference in a drug-free environment. Upon
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