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We present a mathematical model of lophotrichous bacteria, motivated by Pseudomonas putida, which swim through fluid by rotating a cluster of multiple flagella extended from near one pole of the cell body. Although the flagella rotate individually, they are typically bundled together, enabling the bacterium to exhibit three primary modes of motility: push, pull, and wrapping. One key determinant of these modes is the coordination between motor torque and rotational direction of motors. The computational variations in this coordination reveal a wide spectrum of dynamical motion regimes, which are modulated by hydrodynamic interactions between flagellar filaments. These dynamic modes can be categorized into two groups based on the collective behavior of flagella, i.e., bundled and unbundled configurations. For some of these configurations, experimental examples from fluorescence microscopy recordings of swimming P. putida cells are also presented. Furthermore, we analyze the characteristics of stable bundles, such as push and pull, and investigate the dependence of swimming behaviors on the elastic properties of the flagella.
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Multiflagellarity leads to the size-independent swimming speed of peritrichous bacteria
To swim through a viscous fluid, a flagellated bacterium must overcome the fluid drag on its body by rotating a flagellum or a bundle of multiple flagella. Because the drag increases with the size of bacteria, it is expected theoretically that the swimming speed of a bacterium inversely correlates with its body length. Nevertheless, despite extensive research, the fundamental size–speed relation of flagellated bacteria remains unclear with different experiments reporting conflicting results. Here, by critically reviewing the existing evidence and synergizing our own experiments of large sample sizes, hydrodynamic modeling, and simulations, we demonstrate that the average swimming speed ofEscherichia coli, a premier model of peritrichous bacteria, is independent of their body length. Our quantitative analysis shows that such a counterintuitive relation is the consequence of the collective flagellar dynamics dictated by the linear correlation between the body length and the number of flagella of bacteria. Notably, our study reveals how bacteria utilize the increasing number of flagella to regulate the flagellar motor load. The collective load sharing among multiple flagella results in a lower load on each flagellar motor and therefore faster flagellar rotation, which compensates for the higher fluid drag on the longer bodies of bacteria. Without this balancing mechanism, the swimming speed of monotrichous bacteria generically decreases with increasing body length, a feature limiting the size variation of the bacteria. Altogether, our study resolves a long-standing controversy over the size–speed relation of flagellated bacteria and provides insights into the functional benefit of multiflagellarity in bacteria.
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- PAR ID:
- 10506833
- Publisher / Repository:
- Proceedings of the National Academy of Sciences
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences
- Volume:
- 120
- Issue:
- 48
- ISSN:
- 0027-8424
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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We analyse the motion of a flagellated bacterium in a two-fluid medium using slender body theory. The two-fluid model is useful for describing a body moving through a complex fluid with a microstructure whose length scale is comparable to the characteristic scale of the body. This is true for bacterial motion in biological fluids (entangled polymer solutions), where the entanglement results in a porous microstructure with typical pore diameters comparable to or larger than the flagellar bundle diameter, but smaller than the diameter of the bacterial head. Thus, the polymer and solvent satisfy different boundary conditions on the flagellar bundle and move with different velocities close to it. This gives rise to a screening length$$L_B$$within which the fluids exchange momentum and the relative velocity between the two fluids decays. In this work, both the solvent and polymer of the two-fluid medium are modelled as Newtonian fluids with different viscosities$$\mu _s$$and$$\mu _p$$(viscosity ratio$$\lambda = \mu _p/\mu _s$$), thereby capturing the effects solely introduced by the microstructure of the complex fluid. From our calculations, we observe an increased drag anisotropy for a rigid, slender flagellar bundle moving through this two-fluid medium, resulting in an enhanced swimming velocity of the organism. The results are sensitive to the interaction between the bundle and the polymer, and we discuss two physical scenarios corresponding to two types of interaction. Our model provides an explanation for the experimentally observed enhancement of swimming velocity of bacteria in entangled polymer solutions and motivates further experimental investigations.more » « less
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Abstract Lophotrichous bacteria swim through fluid by rotating their flagellar bundle extended collectively from one pole of the cell body. Cells experience modes of motility such as push, pull, and wrapping, accompanied by pauses of motor rotation in between. We present a mathematical model of a lophotrichous bacterium and investigate the hydrodynamic interaction of cells to understand their swimming mechanism. We classify the swimming modes which vary depending on the bending modulus of the hook and the magnitude of applied torques on the motor. Given the hook’s bending modulus, we find that there exist corresponding critical thresholds of the magnitude of applied torques that separate wrapping from pull in CW motor rotation, and overwhirling from push in CCW motor rotation, respectively. We also investigate reoriented directions of cells in three-dimensional perspectives as the cell experiences different series of swimming modes. Our simulations show that the transition from a wrapping mode to a push mode and pauses in between are key factors to determine a new path and that the reoriented direction depends upon the start time and duration of the pauses. It is also shown that the wrapping mode may help a cell to escape from the region where the cell is trapped near a wall.more » « less
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1073/pnas.2310952120
