Swarming on rigid surfaces requires movement of cells as individuals and as a group of cells. For the bacterium Proteus mirabilis, an individual cell can respond to a rigid surface by elongating and migrating over micrometer-scale distances. Cells can form groups of transiently aligned cells, and the collective population is capable of migrating over centimeter-scale distances. To address how P. mirabilis populations swarm on rigid surfaces, we asked whether cell elongation and single-cell motility are coupled to population migration. We first measured the relationship between agar concentration (a proxy for surface rigidity), single-cell phenotypes, and swarm colony phenotypes. We find that cell elongation and single-cell motility are coupled with population migration on low-percentage hard agar (1% to 2.5%) and become decoupled on high-percentage hard agar (>2.5%). Next, we evaluate how disruptions in lipopolysaccharide (LPS), specifically the O-antigen components, affect responses to hard agar. We find that LPS is not essential for elongation and motility of individual cells, as predicted, and instead functions to broaden the range of agar concentrations on which cell elongation and motility are coupled with population migration. These findings demonstrate that cell elongation and motility are coupled with population migration under a permissive range of surface conditions; increasing agar concentration is sufficient to decouple these behaviors. Since swarm colonies cover greater distances when these steps are coupled than when they are not, these findings suggest that collective interactions among P. mirabilis cells might be emerging as a colony expands outwards on rigid surfaces. IMPORTANCE How surfaces influence cell size, cell-cell interactions, and population migration for robust swarmers like P. mirabilis is not fully understood. Here, we have elucidated how cells change length along a spectrum of sizes that positively correlates with increases in agar concentration, regardless of population migration. Single-cell phenotypes can be decoupled from collective population migration simply by increasing agar concentration. A cell’s lipopolysaccharides function to broaden the range of agar conditions under which cell elongation and single-cell motility remain coupled with population migration. In eukaryotes, the physical environment, such as a surface matrix, can impact cell development, shape, and migration. These findings support the idea that rigid surfaces similarly act on swarming bacteria to impact cell shape, single-cell motility, and collective population migration.
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...
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