Abstract
Bacteria often live in biofilms, which are microbial communities surrounded by a secreted extracellular matrix. Here, we demonstrate that hydrodynamic flow and matrix organization interact to shape competitive dynamics in Pseudomonas aeruginosa biofilms. Irrespective of initial frequency, in competition with matrix mutants, wild-type cells always increase in relative abundance in planar microfluidic devices under simple flow regimes. By contrast, in microenvironments with complex, irregular flow profiles - which are common in natural environments - wild-type matrix-producing and isogenic non-producing strains can coexist. This result stems from local obstruction of flow by wild-type matrix producers, which generates regions of near-zero shear that allow matrix mutants to locally accumulate. Our findings connect the evolutionary stability of matrix production with the hydrodynamics and spatial structure of the surrounding environment, providing a potential explanation for the variation in biofilm matrix secretion observed among bacteria in natural environments.
Highlights
In nature, bacteria predominantly exist in biofilms, which are surface-attached or free-floating communities of cells held together by a secreted matrix [1,2,3]
The matrix plays a role in the population dynamics of biofilm-dwelling bacteria [2, 10,11,12,13,14,15]; simulations and experiments using Vibrio cholerae, Pseudomonas fluorescens, and Pseudomonas aeruginosa show that matrix-secreting cell lineages can smother or laterally displace other cell lineages and, in so doing, outcompete neighboring matrix non-producing cells [16,17,18,19,20,21,22,23,24]
Our results show that a feedback process operates between hydrodynamic flow conditions, biofilm spatial architecture, and competition in P. aeruginosa biofilms
Summary
Bacteria predominantly exist in biofilms, which are surface-attached or free-floating communities of cells held together by a secreted matrix [1,2,3]. Our first goal was to compare the population dynamics of the wild type and 75 ∆pelA strains in typical straight-chamber microfluidic devices, which have simple parabolic flow regimes, and in porous environments containing turns and corners, which have irregular flow profiles and better reflect the packed soil environments that P. aeruginosa often occupies [28, 53, 54]. We measured the change in frequency of wild type and ∆pelA cells as a function of their initial ratio in both straight-tunnel chambers and soil-mimicking chambers containing column obstacles From these measurements, we could infer the final stable states of Pel-producing and nonproducing cells as a function of surface topography and flow conditions. In straight-tunnel chambers with simple parabolic flows, wild type PA14 increased in relative abundance regardless of initial population composition, indicating uniform positive selection for Pel secretion This result is consistent with recent studies of V. cholerae and Pseudomonas spp. ∆pelA strain, whose biofilm would otherwise be removed by shear forces, enabling it to proliferate locally using nutrients diffusing from the bulk liquid phase [61]
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