The mechanical world of bacteria

Abstract

In the wild, bacteria are predominantly associated with surfaces as opposed to existing as free-swimming, isolated organisms. They are thus subject to surface-specific mechanics, including hydrodynamic forces, adhesive forces, the rheology of their surroundings, and transport rules that define their encounters with nutrients and signaling molecules. Here, we highlight the effects of mechanics on bacterial behaviors on surfaces at multiple length scales, from single bacteria to the development of multicellular bacterial communities such as biofilms.

Figure 1. Bacteria experience a variety of mechanical effects on surfaces

(A) Flagella, pili, and adhesive substances are useful for attachment of individual bacterial cells to surfaces. Extracellular polymeric substances (EPS) aid in maintaining the integrity of community structures composed of multiple cells. Bacteria use diffusible signaling molecules, chemical weapons, and soluble public goods to interact within such communities. (B) A cell attaching to a surface is subject to a local adhesive force F in the direction normal to the surface. Shear stresses due to fluid flow generate a force F on the cell that is parallel to the surface. Bacteria experience the rheological properties of their surrounding extracellular matrix, which flows and/or deforms upon application of forces. Fluid flow (advection) and Brownian motion (diffusion) transport soluble compounds (black dots) that are released and/or internalized by bacteria.

Figure 2. Influences of environmental mechanics on individual cells and multicellular communities

(A) On surfaces and in the presence of flow, individual bacterial cells use short appendages (fimbriae) and other adhesive structures or substances to remain strongly attached, and (B) they use motorized pili localized at their poles to move against the flow. (C) Bacteria exploit their shapes to orient in flow thereby enhancing surface colonization. (D) At the scale of multicellular communities, bacteria can alter the rheology of the extracellular polymeric substances (EPS) to optimize growth. (E, F) Flow modifies the architecture of bacterial biofilms by driving formation of filamentous structures called streamers, which can obstruct flow but also capture cells and metabolites suspended in the surrounding fluid. (G) Transport of nutrients and other solutes by diffusion and advection drives the growth of and interactions between surface-associated bacteria.

Figure 3. Bacteria leverage fluid flow at the scale of a single cell

(A) E. coli use a catch bond mechanism to enhance attachment to surfaces in flow conditions. (left) Above a critical shear stress, cells are more likely to remain attached to a surface compared to cells that experience lower shear stress, as demonstrated by the peak in the number of adherent cells at finite shear stress (Nilsson et al., 2006). (right)The fimbrial capping protein FimH changes conformation when the fimbria is under tension, thereby increasing its affinity for surface-bound mannose (Le Trong et al., 2010). The mechanics of FimH are analogous to a finger trap toy, where extension enhances binding via twisting. (B) (left) P. aeruginosa attaches to surfaces with polar pili and cells migrate via twitching motility in the direction opposite to the flow. (right) Flow reorients cells in the direction opposite to the flow (Shen et al., 2012); successive pili extensions and retractions promote upstream migration. (C) (left) C. crescentus reorients in the direction of the flow when growing on surfaces (Persat et al., 2014). (right) Hydrodynamic forces act on the curved C. crescentus cell body, attached from one pole, to orient its free pole toward the surface. Thus, new cells are born close to the surface and can better attach immediately following separation from the mother cell. A straight cell dividing in flow has its pole oriented away from the surface, thereby reducing the likelihood of attachment to the surface after separation, which then reduces the rate of surface colonization.

Figure 4. Effect of mechanics on multicellular communities

(A) Photograph and scanning electron micrographs show fluidic channels within biofilms generated by buckling of the EPS matrix (Wilking et al., 2013). Fluid evaporation through the biofilm generates flow within the channels leading to rapid advective transport of nutrients within the biofilm. In the absence of channels, nutrients only slowly diffuse into the biofilm. (B) Fluid flow promotes biofilm extrusions at channel bends that develop into fiber-like streamers extending into the channel centerline (Drescher et al., 2013). These streamers form as channel bends induce localized flow patterns potentially favoring the accumulation of EPS (Rusconi et al., 2011). (C) The interplay between diffusive and advective transport of a nutrient shapes the interactions between “producer” enzyme-secreting cells (yellow) that digest a chitin substrate (blue) and mutant “cheater” cells that do not secrete the chitinase enzyme (red) (Drescher et al., 2014). Without flow, diffusion of liberated chitin oligomers (GlcNac)_n permits “cheater” cells to exploit populations of chitinase-producing cells. In contrast, flow rapidly removes the soluble (GlcNac)_n released from the chitin surface, denying access to “cheaters” and rendering secreted chitinase-production evolutionarily stable.