French researchers discover swimming techniques of deadly plant pathogen

The Phytophtora species are devastating plant pathogens, responsible for billions of dollars of crop damage yearly. Understanding exactly how their zoospores swim at high speed is important in controlling their spread.

A French group of researchers investigated how the two flagella of these tiny (10μm) zoospores interact to propel the organism continuously and efficiently to infect host plants. Their research article was accepted for publication in the journal eLife March 28, and is available in preprint. 

The research group used both experiments and modeling to "show how these two flagella contribute to generate thrust when beating together," and they identify the hairs (mastigonemes) on the anterior flagellum as the "main source of thrust." They also show how the zoospore changes direction by having the posterior flagellum stop while the anterior flagellum changes to a kind of breast stroke to complete a sharp turn.

How they navigate

This is the first study to investigate in detail how the two flagella navigate. The researchers write, "We observe that zoospores can perform long and stable straight runs, discontinued by active turning events. We obtain statistics of the trajectories and develop a numerical model to study and extrapolate the zoospore spreading characteristics solely by random walks. Then, we detail an in-depth study on the hydrodynamics of P. parasitica's flagella and acquire a mathematical model to correlate the functions of two flagella on the motion of straight runs."

Using transmission electron microscopy, the researchers discovered that the flagella have different types of mastigonemes. The anterior flagellum has two kinds of hairs, straight and tubular, and curved longer and thicker. These hairs are randomly distributed.

In contrast the posterior flagellum is a "smooth whip shape with plenty of very fine hairs on the surface." These hairs, they write, "wrap around the flagellum to increase the contact surface, thus increasing the propulsion efficiency."

Zoospore `swimming pool'

To study how the zoospores swim, the researchers created a "swimming pool" for them, a thin film of water on a glass slide. They then took videos of the zoospores in action. From these they were able to calculate swimming speed, straight runs and turnings. They were able to observe how the flagella interacted to generate speed and the changes in direction. 

From their observations they developed a mathematical model using resistive force theory to predict the propulsive force and velocity. Their model takes into account the different behavior of each flagellum. They write, "Overall we show that the energy is shared in comparable manner between two flagella, but the anterior flagellum has more influence on zoospore speed, power consumption and propelling efficiency."

"On the other hand, the posterior flagellum provides a modest contribution to zoospore speed despite beating at higher frequency and consuming half the energy," they added.

The researchers speculate that because the function of the posterior flagellum is not completely clear in helping with thrust and turning, "it might contribute to other physical activities such as chemical and electrical sensing," they said, adding it might provide "an anchor-like turning point for zoospore, instead of acting like a rudder as previously hypothesized."

“Our study is a fundamental step toward a better understanding of the spreading of plant pathogens' motile forms, and shows that the motility pattern of these biflagellated zoospores represents a distinct eukaryotic version of the celebrated 'run-and-tumble' motility class exhibited by peritrichous [having multiple flagella] bacteria,” they said.

The authors conclude that their discoveries "pave new ways" to target each flagellum and help control the devastating diseases these zoospores cause.

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Quang D. Tran et al., "Coordination of two opposite flagella allows high-speed swimming and active turning of individual zoospores," eLife preprint (2022). DOI: 10.7554/eLife.71227