Bacteria Navigate Anisotropic Media using a Flagellar Tug-of-Oars

Abstract

Bacteria thrive in anisotropic media such as biofilms, biopolymer solutions, and soil pores. In strongly mechanically anisotropic media, physical interactions force bacteria to swim along a preferred direction rather than to execute the three-dimensional random walk due to their run-and-tumble behavior. Despite their ubiquity in nature and importance for human health, there is little understanding of bacterial mechanisms to navigate these media while constrained to one-dimensional motion. Using a biocompatible liquid crystal, we discovered two mechanisms used by bacteria to switch directions in anisotropic media. First, the flagella assemble in bundles that work against each other from opposite ends of the cell body, and the dominating side in this flagellar “Tug-of-Oars” propels the bacterium along the nematic direction. Bacteria frequently revert their swimming direction <a:math xmlns:a="http://www.w3.org/1998/Math/MathML"><a:msup><a:mn>180</a:mn><a:mo>∘</a:mo></a:msup></a:math> by a mechanism of flagellar buckling and reorganization on the opposite side of the cell. The Frank elastic energies of the liquid crystal dictate the minimum compression for the Euler buckling of a flagellum. Beyond a critical elasticity of the medium, flagellar motors cannot generate the necessary torque for flagellar buckling, and bacteria are stuck in their configuration. However, we found that bacteria can still switch swimming directions using a second mechanism where individual bundles alternate their rotation. Our results shed light on bacterial strategies to navigate anisotropic media and give rise to questions about sensing environmental cues and adapting at the level of flagellar bundles. The two adaptation mechanisms found here support the use of biocompatible liquid crystals as a synthetic model for bacterial natural environments. Published by the American Physical Society 2024