Swarming bacteria respond to increasing barriers to motility by increasing cell length and modifying colony structure

Abstract

Organisms can alter morphology and behaviors in response to environmental stimuli such as mechanical forces exerted by surface conditions. The bacterium Proteus mirabilis responds to surface-based growth by enhancing cell length and degree of cell-cell interactions. Cells grow as approximately 2-micrometer rigid rods and independently swim in liquid. By contrast on hard agar surfaces, cells elongate up to 40-fold into snake-like cells that move as a collective group across the surface. Here we have elucidated that individual cell size and degree of cell-cell interactions increased across a continuous gradient that correlates with increasing agar density. We further demonstrate that interactions between the lipopolysaccharide (LPS) component of the outer membrane and the immediate local environment modified these responses by reducing agar-associated barriers to motility. Loss of LPS structures corresponded with increased cell elongation on any given surface. These micrometer-scale changes to cell shape and collective interactions corresponded with centimeter-scale changes in the overall visible structure of the swarm colony. It is well-appreciated in eukaryotes that mechanical forces impact cell shape and migration. Here we propose that bacteria can also dynamically respond to the mechanical forces of surface conditions by altering cell shape, individual motility, and collective migration. IntroductionEukaryotic and prokaryotic cells undergo alterations, including changes in cell morphology and collective behaviors, in response to interactions with the physical environment. For example, robust swarmers such as the human pathogens Proteus mirabilis and Vibrio parahaemolyticus (1) can swim as short, rigid rod-shaped cells in liquid and through low-density (0.3%) agar. On low-wetness and highdensity agar (0.75% to 2.5%), these bacteria elongate dramatically and move as a collective group on top of the surface. By comparison, the swarm motility of temperate swarmers such as Escherichia coli or Salmonella enterica is generally restricted to low-density agar (< 0.7%) or high wetness Eiken agar (reviewed in (2, 3)). For all of the aforementioned bacteria, flagella power the motility in liquid and on surfaces. Furthermore, a transition from swimming to swarming coincides with a series of large-scale transcriptional changes triggered by contact between flagella and a surface (Figure 1) (4-12).Here we utilize P. mirabilis as a tractable model for exploring how morphology and cell-cell interactions respond to the surface. P. mirabilis cells are approximately 2-µm long, rigid, and rod-shaped in liquid. Such cells swim independently, resulting in a visible uniform haze to the structure of the swim colony. Upon contact with a hard surface (Figure 1), these rigid, rod-shaped cells can elongate up to 40-fold into a flexible, snake-like, hyper-flagellated swarmer cell (13,14) that has a distinctive gene expression profile (15). P. mirabilis swarmer cells are thought to bundle their flagella to facilitate cooperative swarm motil...

Biofilms 2018: a Diversity of Microbes and Mechanisms

“…The dynamics of the interactions between self and nonself are readily apparent in the oscillatory (bullseye) patterns of swarmer cell migration, where mixtures of strains eventually result in self-only cells on the outer edges of the swarm. These patterns and local dynamics change as the agar concentration increases, indicating that these cells integrate cues from both their cellular neighbors and the environmental conditions (84).…”