Self-Driven Jamming in Growing Microbial Populations

Abstract

In natural settings, microbes tend to grow in dense populations [1][2][3][4] where they need to push against their surroundings to accommodate space for new cells. The associated contact forces play a critical role in a variety of population-level processes, including biofilm formation [5][6][7], the colonization of porous media [8,9], and the invasion of biological tissues [10][11][12]. Although mechanical forces have been characterized at the single cell level [13][14][15][16], it remains elusive how collective pushing forces result from the combination of single cell forces. Here, we reveal a collective mechanism of confinement, which we call self-driven jamming, that promotes the buildup of large mechanical pressures in microbial populations. Microfluidic experiments on budding yeast populations in space-limited environments show that self-driven jamming arises from the gradual formation and sudden collapse of force chains driven by microbial proliferation, extending the framework of driven granular matter [17][18][19][20]. The resulting contact pressures can become large enough to slow down cell growth, to delay the cell cycle in the G1 phase, and to strain or even destroy the microenvironment through crack propagation. Our results suggest that self-driven jamming and build-up of large mechanical pressures is a natural tendency of microbes growing in confined spaces, contributing to microbial pathogenesis and biofouling [21][22][23][24][25][26].

Cellular packing, mechanical stress and the evolution of multicellularity

“…Decreasing volume fraction may decrease the number of contacts between cells, reducing the amount of internal stress, as previously observed in collections of grains 18 and unicellular yeast 17 . Thus, by reducing the number of cell-cell interactions in week-8 clusters, decreasing volume fraction may also reduce the rate of internal stress accumulation.…”

“…Finally, we measured the compressive modulus of clusters of both genotypes. Previous studies demonstrated that the elastic modulus of individual yeast cells is relatively constant with respect to cell size 16 ; if individual snowflake yeast cells behave similarly, the compressive modulus may be expected to increase if interior volume fraction increases 17,18 . It is important to note that the distribution of cells within clusters is very heterogeneous 7,19 ; cells in the cluster interior are much more crowded than those at the periphery (Fig.…”

Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer

“…The idea of phase transition has recently been proposed to explain the collective motility of many-cell systems such that increasing cell density would lead to glass transition that globally jams the systems' motion (41)(42)(43)(44). Our results may suggest a similar "disorder-to-order" transition in collective cell oscillations such that some critical cell population is required to ensure spatiotemporally organized, aligned, and polarized cell oscillations in the amnioserosa tissue.…”

Modeling mechanical interactions in growing populations of rod-shaped bacteria

“…Agent-based models, therefore, need to be able to model the force exerted by growing cells, as well as the mechanical interactions induced by cell-cell contacts or contact with environmental boundaries. Further, it has been shown that the environment of an individual cell can influence its growth, which in turn influences the collective’s behavior through mechanical communication [8, 10, 14, 27, 34]. In particular, mechanical confinement can cause cells within the collective to grow at different rates [8, 10].…”