Colloquium: Magnetotactic bacteria: From flagellar motor to collective effects

Magnetotactic bacteria are swimming microorganisms able to follow magnetic field lines with the help of an organelle called the magnetosome that is made of biomineralized magnetic crystals assembled in a chain. In combination with this ability, these bacteria perform active oxygen sensing to reach the oxic-anoxic transition zone, which is often located in the upper part of the sediment. From a physicist’s perspective, magnetotactic bacteria can be seen at the interface between bacterial active matter and magnetic colloids, which gives them unique properties at both the individual and collective levels. In crowded media and/or when they are submitted to external flows, their motion can be efficiently driven by magnetic fields, which leads to surprising effects. In this Colloquium, the different features of magnetotactic bacteria at are reviewed at every scale, from single cell to collective motion, from simple to complex environments, and by emphasizing the differences from other bacterial species or passive magnetic colloids. The Colloquium concludes with a discussion of perspectives on using magnetotactic bacteria in active magnetorheology.

Figure 1

TEM image of a MTB with the magnetosome chain.

Figure 2

(a) BFM diagram. From Mariana Ruiz Villarreal. (b) MO-1 flagellar motor architecture. The intertwined hexagonal array consists of the basal bodies of seven flagella and 24 fibrils, with large brown and small yellow-green circles overlaid on the flagellar and fibril basal bodies, respectively. From [155].

Figure 3

Flow streamlines for (a) a force dipole of pusher type, (b) a source dipole, and (c) a force dipole plus source dipole. Data were calculated using the PyStokes python library ([166]).

Figure 4

The main morphologies and flagellar apparatus of MTBs (scale differences are not respected).

Figure 5

(a) The average of the cosine of the angle between $m$, the magnetic moment, and the external field is given by the Langevin function and corresponds to the paramagnetic model. (b) The experimental orientation distribution of the magnetic moment of MTBs measured with an external field of $B=0.3\mathrm{mT}$ and fitted with Eq. (9) for $T=300\mathrm{K}$. From [134], and [94].

Figure 6

Swimming trajectories of MTBs through a homogeneous porous micromodel (a) in the absence of and (b) in the presence of an applied magnetic field of 0.3 mT, with the corresponding polar graphs of progressive velocities overlaid in the center in (c) and (d). From [199].

Figure 7

(a) Competition between the hydrodynamic ($L_H$) and magnetic ($L_M$) torques controls the transitions between the toplike states (the body in the solid line) and orbitlike states (the body in the dashed line) when the field $\mathbf{B}$ is oriented perpendicularly to the surface. (b) Rolling forces on the cell body $F_y^b$ and the flagellum $F_y^f$ lead to circular swimming of the bacteria at the surface. (c),(d) Cell swimming under the purely in-plane field $B_x$, where $F_y^b=F_y^f$. (e),(f) Cell oriented at an angle ${\theta }_H$ relative to the surface. (f) As the cell is tilted out of plane, $F_y^f$ is attenuated, yielding an unbalanced hydrodynamic force in the $y$ direction, causing the bacterium to swim toward the left of the image. From [144].

Figure 8

Top row: experimentally measured cell trajectories in a corrugated channel with counterflow. The gray arrows indicate the direction of the bacterial transport. The scale $\mathrm{bar}=40\mathrm{\mu }\mathrm{m}$. Bottom row: Langevin simulations. $\mathrm{\Phi }$ is the ratio between the maximum flow speed and the bacterial swimming speed ([190]).

Figure 9

Magnetotaxis in the oxic-anoxic transition zone (OATZ). The gray bacteria containing a magnetosome chain correspond to magnetotactic bacteria swimming along Earth’s magnetic field lines, while the gray bacteria without a chain of magnetosome correspond to nonmagnetotactic bacteria that swim randomly From [61].

Figure 10

(a) Band formation in a capillary assay where one end is sealed (the anoxic end) and the other end is open, allowing for oxygen diffusion (the oxic end). (b) Different types of magneto-aerotactic behavior. From [107].

Figure 11

Diagram of the microfluidic setup allowing the dynamic change of the oxygen gradient inside the chamber containing the cells. From [108].

Figure 12

Density projections averaged along the $y$ axis from 3D nonlinear simulations at different time steps for pusher (top row) and puller swimmers (bottom row) in the unstable regime. From [96].

Figure 13

(a) Self-assembled clusters of MTBs viewed from the top. The computable information density for a population was subjected to 10–100 G (1–10 mT) fields for 55 s toward the surface. As the field is decreased, the extent of the decay reduces until it remains nearly static in time for low values. Inset: selected microscopy images from the self-organization process associated with the red curve. (b) Self-assembled clusters of MTBs viewed from the side, where the magnetic field points toward the bottom surface. A uniform distribution of bacteria accumulates near the wall, and the concentration instability emerges. At longer times, plumes grow and cluster until a steady flow is obtained at $t=2\min$. From [146], and [182].

Figure 14

(a) Image of a rotating crystal made of synthetic magnetic microswimmers. Particles with polar alignment and a single angular frequency can self-organize into (b) rotating macrodroplets and (c) microflock patterns. Differences in color indicate different orientations. From [109], and [186].

Figure 15

(a) Phase diagram of the instability for various values of $V_f$ and $B$. The red (dark gray) dots are the unstable jets, whereas the green (light gray) dots are the stable jets. The black line is the best adjustment with $V_f=a/B+c$, with $a=0.630\mathrm{mm}\mathrm{mT}{\mathrm{s}}^{-1}$ and $c=0.19\mathrm{mm}{\mathrm{s}}^{-1}$. Adapted from [191]. (b) Theoretical phase diagram in the $(T_{\mathrm{eff}}/T_c,J,{\varphi }_c)$ parameter space showing the focusing (triangles), pearling (dots), and condensation (squares). From [129].

Figure 16

Variation of the viscosity of an E. coli suspension as a function of the volume fraction of bacteria in oxygenated conditions (filled symbols) and deoxygenated conditions (empty symbols). From [115].

Figure 17

Particle shear stress as a function of the hydrodynamic Péclet number for a fixed ${\mathrm{Pe}}_M=1$ fixed particle activity value $A=10$. From [189].

Figure 18

Disturbance flow generation by a magnetic field. Left sketch: average particle distribution and orientation in the absence of a magnetic field. $B=B\mathbf{x}$ is a uniform magnetic field with a unit vector $h$, $\overrightarrow{m}$ is the magnetic moment of the particle, $\mathrm{\Phi }$ corresponds to the angle of the magnetic field, $u$ is the fluid velocity, and $D$ is the second orientational moment of the distribution function representing the nematic alignment of the cells. Right sketch: flow created by the combined effect of a magnetic field and active stresses on a suspension of pusher microswimmers. In the case of puller microswimmers, the magnetic stress remains the same, while the sign of the active disturbance flow changes. From [4].