Escherichia coli swimming is robust against variations in flagellar number

• Published in: eLife Vol. 3; p. e01916
• Main Authors: Mears, Patrick J, Koirala, Santosh, Rao, Chris V, Golding, Ido, Chemla, Yann R
• Format: Journal Article
• Language: English
• Published: England eLife Sciences Publications Ltd 11.02.2014; eLife Sciences Publications, Ltd
• Subjects: bacterial chemotaxis; Bacterial Proteins - genetics; Bacterial Proteins - metabolism; Bias; Biophysics and Structural Biology; Chemotaxis; CheY protein; E coli; Escherichia coli; Escherichia coli - genetics; Escherichia coli - metabolism; Escherichia coli - physiology; Escherichia coli Proteins; Flagella; Flagella - physiology; Genotype; Locomotion; Membrane Proteins - genetics; Membrane Proteins - metabolism; Methyl-Accepting Chemotaxis Proteins; Microbiology and Infectious Disease; Models, Biological; Mutation; optical tweezer; Phenotype; Simulation; single-cell studies; Stochastic Processes; Swimming; Swimming behavior; flagella; optical tweezers; bacterial chemotaxis; single-cell studies
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.01916

Bacterial chemotaxis is a paradigm for how environmental signals modulate cellular behavior. Although the network underlying this process has been studied extensively, we do not yet have an end-to-end understanding of chemotaxis. Specifically, how the rotational states of a cell’s flagella cooperatively determine whether the cell ‘runs’ or ‘tumbles’ remains poorly characterized. Here, we measure the swimming behavior of individual E. coli cells while simultaneously detecting the rotational states of each flagellum. We find that a simple mathematical expression relates the cell’s run/tumble bias to the number and average rotational state of its flagella. However, due to inter-flagellar correlations, an ‘effective number’ of flagella—smaller than the actual number—enters into this relation. Data from a chemotaxis mutant and stochastic modeling suggest that fluctuations of the regulator CheY-P are the source of flagellar correlations. A consequence of inter-flagellar correlations is that run/tumble behavior is only weakly dependent on number of flagella. Escherichia coli is a rod-shaped bacterium commonly found in the lower intestines of humans and other warm-blooded animals. While most strains of E. coli are harmless, including most of those found in the human gut, some can cause diseases such as food poisoning. Due to its close association with humans and the fact that it is easy to grow and work with in the laboratory, E. coli has been intensively studied for over 60 years. Many bacteria are capable of ‘swimming’ by using one or more flagella. These rotating whip-like structures are each driven by a reversible motor, and they act a bit like a propeller on a boat. While some bacteria have only a single flagellum, others, such as E. coli, have multiple flagella distributed over the cell surface. Rotating all their flagella in a counterclockwise direction allows the bacterium to swim—and it has been proposed that the clockwise movement of at least one flagellum will cause the bacterium cell to stop swimming and start tumbling. E. coli is able to control the time it spends swimming or tumbling to move towards a nutrient, such as glucose, or away from certain harmful chemicals. However, the details of how the number of flagella and the direction of rotation (clockwise or counterclockwise) influence the motion of the bacterium are not fully understood. Now, Mears et al. have used ‘optical tweezers’ to immobilize individual E. coli cells under a microscope, and then track both their swimming behavior and the movements of their flagella. This revealed that the individual flagella on the same cell tend to move in a coordinated way. Therefore, whilst tumbling could be caused by a single flagellum stopping swimming behavior, it often involved a concerted effort by many of the cell’s flagella. After observing that E. coli cells with more flagella spent less time tumbling than would be predicted if a single flagella always ‘vetoed’ swimming, Mears et al. propose a new mathematical relationship between the number of flagella on the cell, the direction of rotation, and the resulting probability that the cell will tumble. This work shows that swimming behavior in bacteria is less affected by variations in the number of flagella than previously thought—and this phenomenon may provide evolutionary advantages to E. coli. The next step is to explore the mechanism by which bacteria coordinate their flagella.