Bacterial biomechanics-From individual behaviors to biofilm and the gut flora

Abstract

Bacteria inhabit a variety of locations and play important roles in the environment and health. Our understanding of bacterial biomechanics has improved markedly in the last decade and has revealed that biomechanics play a significant role in microbial biology. The obtained knowledge has enabled investigation of complex phenomena, such as biofilm formation and the dynamics of the gut flora. A bottom-up strategy, i.e., from the cellular to the macroscale, facilitates understanding of macroscopic bacterial phenomena. In this Review, we first cover the biomechanics of individual bacteria in the bulk liquid and on surfaces as the base of complex phenomena. The collective behaviors of bacteria in simple environments are next introduced. We then introduce recent advances in biofilm biomechanics, in which adhesion force and the flow environment play crucial roles. We also review transport phenomena in the intestine and the dynamics of the gut flora, focusing on that in zebrafish. Finally, we provide an overview of the future prospects for the field.

FIG. 1.

Schematic of a bottom-up understanding of bacterial biomechanics from the cellular to the macroscale. Top left, Escherichia coli cell; top middle, trajectories of tracers in a dense E. coli suspension; top right, zebrafish larva; and bottom right, fluorescent tracer particles in the intestine of zebrafish larva. The complexity of biomechanics increases with scale.

FIG. 2.

Schematics of a puller and a pusher. The puller has a flagellum in front of the cell body, while the pusher has a flagellum behind the cell body.

FIG. 3.

Collective motion of bacteria in a dense suspension. (a) Numerical simulation of collective swimming of prolate squirmers in a monolayer suspension. Yellow arrows, velocity vectors; and gray lines, orientations. The areal fraction of cells is 0.3, and the cells are pushers (β = −0.3). (Problem settings are identical to Kyoya et al., 2015.). (b) Trajectories of tracer particles in a dense E. coli suspension. Scale bar, 50 μm. (Settings are identical to Ishikawa et al., 2011.)

FIG. 4.

Schematics of the stress field generated by pushers. (a) A pusher with the given orientation helps the wall movement, and thus the shear viscosity is decreased. (b) Normal stress appears when orientation of pushers is anisotropic.

FIG. 5.

Particle-based simulation of the biofilm. A bacterial suspension flows through blocks, and streamers are formed on the downstream side. Spheres represent individual bacteria that have adhered to each other and the blocks.

FIG. 6.

Mechanical roles of anterograde and retrograde intestinal peristalsis in zebrafish larva. (a) Péclet numbers after injection of food into the anterior and posterior intestine. (b) Schematic of food mixing and advection in the zebrafish larval intestine. AI, anterior intestine; MI, middle intestine; PI, posterior intestine; and An, anus. Reproduced with the permission from Kikuchi et al., Am. J. Physiol. 318, G1013–G1021 (2020). Copyright 2020 APS.

FIG. 7.

Simulation of the gut flora of a zebrafish larva. (a) Three-dimensional geometry of the intestine. (b) Pressure distribution and velocity vectors. White arrows, retrograde and anterograde peristalsis. (c) Nutrient distribution. (d) Bacterial distribution without taxis. (e) Bacterial distribution with taxis. Reproduced with the permission from Yang et al., J. Theor. Biol. 446, 101–109 (2018). Copyright 2018 Elsevier.