Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms

  • Nadell C
  • Ricaurte D
  • Yan J
  • et al.
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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.Bacteria often live together – attached to surfaces like river rocks, water pipes, the lining of the gut and catheters – in communities called biofilms. These groups of bacteria are small-scale ecosystems in which cells cooperate and compete with one another to obtain resources, such as food and space to grow. Within a biofilm, a sticky glue-like substance called the matrix binds the cells to each other and to the surface. Cells that make the matrix typically have an advantage over those that do not because they can better resist the shearing forces experienced when liquid flows over the surface. The matrix also helps cells to capture nutrients from the passing liquid. Nevertheless, not all strains of bacteria make matrix, despite its advantages.Because of where they can grow, biofilms are fundamentally important in the environment, in industry and in infections. Resolving why some bacteria make matrix while others do not could therefore allow scientists and engineers to re-design the surfaces involved in these settings to discourage harmful biofilms or to encourage beneficial ones.Nadell, Ricaurte et al. have now used a bacterium called Pseudomonas aeruginosa to explore how the properties of the surface and the flowing liquid affect matrix production among cells in biofilms. P. aeruginosa typically lives in soil and can cause infections in people, especially in hospital patients and people who have weakened immune systems. Nadell, Ricaurte et al. studied normal P. aeruginosa bacteria and a mutant strain that is unable to make matrix. The strains were labeled with fluorescent markers and put into special chambers that simulated different environments. The proportion of each strain was measured after three days of biofilm growth. When biofilms were grown under flowing liquid in simple environments with flat surfaces, matrix producers always outcompeted non-producers. However, the two strains coexisted in more complex and porous environments, like those found in soil.Nadell, Ricaurte et al. went on to show that the strains could co-exist because the matrix producers made biofilms that created areas within the environment where the liquid flows very slowly or not at all. In these regions, non-producing cells could compete successfully because resistance to shearing forces is less important when flow is weak or absent, and so the non-producing cells were not washed away. The results begin to explain why matrix production among cells in environmental settings is diverse and highlight that the environment is important in the evolution of bacterial biofilms.

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Nadell, C. D., Ricaurte, D., Yan, J., Drescher, K., & Bassler, B. L. (2017). Flow environment and matrix structure interact to determine spatial competition in Pseudomonas aeruginosa biofilms. ELife, 6. https://doi.org/10.7554/elife.21855

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