Abstract
Unraveling bacterial strategies for spatial exploration is crucial for understanding the complexity in the organization of life. Bacterial motility determines the spatiotemporal structure of microbial and controls infection spreading and the microbiota organization in guts or in soils. Most theoretical approaches for modeling bacterial transport rely on their run-and-tumble motion. For Escherichia coli, the run-time distribution is reported to follow a Poisson process with a single characteristic time related to the rotational switching of the flagellar motors. However, direct measurements on flagellar motors show heavy-tailed distributions of rotation times stemming from the intrinsic noise in the chemotactic mechanism. Currently, there is no direct experimental evidence that the stochasticity in the chemotactic machinery affects the macroscopic motility of bacteria. In stark contrast with the accepted vision of run and tumble, here we report a large behavioral variability of wild-type E. coli, revealed in their three-dimensional trajectories. At short observation times, a large distribution of run times is measured on a population and attributed to the slow fluctuations of a signaling protein triggering the flagellar motor reversal. Over long times, individual bacteria undergo significant changes in motility. We demonstrate that such a large distribution of run times introduces measurement biases in most practical situations. Our results reconcile the notorious conundrum between run-time observations and motor-switching statistics. We finally propose that statistical modeling of transport properties, currently undertaken in the emerging framework of active matter studies, should be reconsidered under the scope of this large variability of motility features.
1 More- Received 6 January 2020
- Accepted 26 February 2020
- Corrected 10 November 2020
DOI:https://doi.org/10.1103/PhysRevX.10.021004
Published by the American Physical Society under the terms of the Creative Commons Attribution 4.0 International license. Further distribution of this work must maintain attribution to the author(s) and the published article’s title, journal citation, and DOI.
Published by the American Physical Society
Physics Subject Headings (PhySH)
Corrections
10 November 2020
Correction: In the first paragraph of Sec. IV C, the expression for was presented incorrectly and has been set right.
Popular Summary
Bacterial motion determines the changing structure of microbial communities and controls infection spreading as well as microbiota organization in ecosystems. E. coli bacteria explore their environment using a “run-and-tumble” strategy: a sequence of straight paths (runs) and sudden changes in swimming direction (tumbles) that happen when motors driving the cell’s tail-like flagellum change rotation direction for a short time. While this random walk is classically described as a process with a single characteristic run time, the flagellar motor rotation switching, responsible for reorientations, displays a wide distribution of times. To address this paradox, we built a 3D tracking microscope suited to follow swimming bacteria for as long as tens of minutes.
Our results reconcile individual motor rotation and bacterial spatial exploration in three dimensions. We reveal a continuous variation of exploration “moods” for individual bacteria, characterized by periods of frequent directional changes alternating with periods of persistent swimming. The dynamics can be explained by important fluctuations in the number of certain proteins inside the cell that are responsible for the motor switching.
Future research will address the importance of these realistic run-and-tumble statistics in the macroscopic transport of bacteria. Bacterial persistent swimming may help to explain the onset of medical emergencies as well as bacterial anomalous transport in confined environments, such as narrow capillaries and porous media. This knowledge could be relevant to emerging technologies for targeted drug delivery or for understanding the spreading of biocontaminants in soils.