Bacterial rheotaxis

Abstract

The motility of organisms is often directed in response to environmental stimuli. Rheotaxis is the directed movement resulting from fluid velocity gradients, long studied in fish, aquatic invertebrates, and spermatozoa. Using carefully controlled microfluidic flows, we show that rheotaxis also occurs in bacteria. Excellent quantitative agreement between experiments with Bacillus subtilis and a mathematical model reveals that bacterial rheotaxis is a purely physical phenomenon, in contrast to fish rheotaxis but in the same way as sperm rheotaxis. This previously unrecognized bacterial taxis results from a subtle interplay between velocity gradients and the helical shape of flagella, which together generate a torque that alters a bacterium's swimming direction. Because this torque is independent of the presence of a nearby surface, bacterial rheotaxis is not limited to the immediate neighborhood of liquid-solid interfaces, but also takes place in the bulk fluid. We predict that rheotaxis occurs in a wide range of bacterial habitats, from the natural environment to the human body, and can interfere with chemotaxis, suggesting that the fitness benefit conferred by bacterial motility may be sharply reduced in some hydrodynamic conditions.

Fig. 1.

Bacterial chemotaxis and rheotaxis. (A) Many bacteria can climb chemical gradients by chemotaxis, for example to seek high nutrient concentrations. (B) Ambient velocity gradients can also affect motility, potentially hampering chemotaxis by orienting bacteria away from nutrient sources. The x–y plane is the flow gradient plane, defined by the direction of the flow (x) and the direction of the flow velocity gradient (y). (C) The mechanism responsible for bacterial rheotaxis, shown for a cell with a left-handed flagellum. The chirality of the flagellum causes a lift force along +z. This force is opposed by the drag on the cell body, producing a torque on the cell. This torque reorients the bacterium, which therefore has a component V of its swimming velocity U directed along –z. V is the rheotactic velocity.

Fig. 2.

B. subtilis OI4139 exhibits rheotaxis. The rheotactic velocity, V, normalized by the mean swimming speed, U (55 μm⋅s⁻¹), is shown as a function of the shear rate, S. (A) Data obtained one-quarter depth above the bottom of the microchannel. Open symbols of different colors refer to six replicate experiments (Materials and Methods). Black solid squares with bars denote the mean and SD of the six replicates. The solid line is the model prediction for a cell body radius of a = 0.5 μm and flagellar morphology corresponding to the flagellar bundle of B. subtilis (Materials and Methods). (Inset) Schematic of the coordinate system, flow, and bacterial motility. (B) Data obtained one-quarter depth below the top (red and pink) and one-quarter depth above the bottom (green and cyan) of the microchannel show an equal and opposite rheotactic velocity, V, because the shear rate S is equal in magnitude and opposite in sign at these two depths. Open symbols refer to two replicate experiments and solid symbols denote the mean of the two replicates.

Fig. 3.

Predicted rheotactic velocity. A mathematical model reveals the mechanism behind bacterial rheotaxis. The rheotactic velocity, V, is plotted relative to the mean swimming speed, U (55 μm⋅s⁻¹), as a function of the shear rate, S. SS refers to smooth-swimming bacteria, with a cell body of radius a. RT refers to bacteria that run and tumble. NM refers to nonmotile bacteria. EL refers to a hypothetical ellipsoid moving along its major axis at a constant speed relative to the fluid (i.e., a nonchiral swimmer). All model bacteria (SS, RT, and NM) have the same flagellar morphology, corresponding to the flagellar bundle of B. subtilis.

Fig. 4.

Bacteria do not change swimming speed in response to shear. The mean speed of a population of bacteria, U, is shown before and after exposure to shear. Bars denote the SD among five replicate experiments and solid lines indicate speed before exposure to shear. The shear rate was S = 500 s⁻¹.