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Coordination of two opposite flagella allows high-speed swimming and active turning of individual zoospores - PubMed

  • ️Sat Jan 01 2022

Coordination of two opposite flagella allows high-speed swimming and active turning of individual zoospores

Quang D Tran et al. Elife. 2022.

Abstract

Phytophthora species cause diseases in a large variety of plants and represent a serious agricultural threat, leading, every year, to multibillion dollar losses. Infection occurs when their biflagellated zoospores move across the soil at their characteristic high speed and reach the roots of a host plant. Despite the relevance of zoospore spreading in the epidemics of plant diseases, individual swimming of zoospores have not been fully investigated. It remains unknown about the characteristics of two opposite beating flagella during translation and turning, and the roles of each flagellum on zoospore swimming. Here, combining experiments and modeling, we show how these two flagella contribute to generate thrust when beating together, and identify the mastigonemes-attached anterior flagellum as the main source of thrust. Furthermore, we find that turning involves a complex active process, in which the posterior flagellum temporarily stops, while the anterior flagellum keeps on beating and changes its gait from sinusoidal waves to power and recovery strokes, similar to Chlamydomonas's breaststroke, to reorient its body to a new direction. 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 bacteria.

Keywords: biflagellated microswimmers; infectious disease; microbiology; p. parasitica; physics of living systems; phytophthora diseases; zoospores.

Plain language summary

Microorganisms of the Phytophthora genus are serious agricultural pests. They cause diseases in many crops, including potato, onion, tomato, tobacco, cotton, peppers, and citrus. These diseases cause billions of dollars in losses each year. Learning more about how the tiny creatures disseminate and reach host plants could help scientists develop new ways to prevent such crop damage. The spore cells of Phytophthora, also known as zoospores, have two appendages called flagella on their bodies. A tinsel-shaped flagellum is near the front of the creature and a long smooth filament-like flagellum is near the posterior. Zoospores use their flagella to swim at high speeds through liquid toward potential plant hosts. Their complex swimming patterns change in response to different physical, chemical, and electrical signals in the environment. But exactly how they use their flagella to generate these movements is not clear. Tran et al. reveal new details about zoospore locomotion. In the experiments, Tran et al. recorded the movements of zoospores in a tiny ‘swimming pool’ of fluid on top of a glass slide and analyzed the movements using statistical and mathematical models. The results uncovered coordinated actions of the flagella when zoospores swim in a straight line and when they turn. The tinsel-like front flagellum provides most of the force that propels the zoospore forward. To do this, it beats with an undulating wave pattern. It shifts the beating to a breast-stroke pattern to change direction. The posterior flagellum provides a smaller forward thrust and temporarily pauses during turns. The study provides new details about zoospore’s movements that may help scientists develop new strategies to control these pests. It also offers more information about how flagella coordinate their actions to switch speeds or change directions that may be of interest to other scientists studying organisms that use flagella to move.

© 2022, Tran et al.

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Conflict of interest statement

QT, EG, PT, CC, FO, FP, XN No competing interests declared

Figures

Figure 1.
Figure 1.. Characteristics of P. parasitica zoospore.

(A) Swimming of zoospores in comparison with different prokaryotic and eukaryotic microswimmers. Black arrows indicate the swimming direction of the swimmers. (B) Scanning electron microscopy images of the zoospore. The insets show the enlarged images of the cell body and the two flagella. (C) Transmission electron microscopy images with negative staining. (1) Image of the zoospore showing the different structures of the two flagella. The anterior has multiple mastigonemes, while the posterior has a smooth straight structure. (2) Close zoom-in image of the anterior flagellum. It is noticed that there are two types of mastigonemes on this flagellum: one with straight tubular shape, the other with non-tubular shape but longer and bigger in size. (3) Close zoom-in image of the posterior flagellum. There are plenty of thin and short hairs wrapping along the flagellum and several non-tubular mastigonemes appearing near the cell body. (4) The non-tubular mastigonemes. (5) The tubular mastigonemes with tiny hairs at the tips.

Figure 2.
Figure 2.. Swimming trajectories of P. parasitica zoospores.

(A) Trajectories of zoospores swimming in water captured from the microscopic assay for 60 s. Sample size N=58. Note: not all trajectories are shown. Each position of the zoospores is captured every Δ⁢t=0.0167⁢s. The trajectories are smoothed with moving average (step length n=12). (B) The progression of speed U and (C) moving directions θ over time of a single zoospore extracted from the population in the assay. (D) Distribution of zoospore speed p⁢(U). (E) Polarity distribution of moving direction p⁢(θ). (F) Survival curves p⁢(τ≥t) of the running time τr and stopping time τs. (G) Distribution of turning angle p⁢(Δ⁢θ), with positive angle values indicating counter-clockwise, and negative as clockwise direction. (H) Schematics showing the strategy of the simulation model of zoospores swimming in water. (I) The estimated mean squared displacement (MSD) over time intervals t, constructed from the simulation data. The inset compares the experimental data and simulation of MSD at the experimental time-scale of 60 s. By simulation, at long time scale of 1 h, MSD of zoospores shows a diffusion of Brownian particles with the diffusion coefficient D=3.5×10-4⁢cm2⁢s-1.

Figure 3.
Figure 3.. Theoretical model of swimming individual P. parasitica zoospore.

(A) Images of an individual zoospore swimming with two flagella beating in sinuisoidal waveform shapes and its cell body gyrating with rate ϕ˙ while moving forward with speed U. The combined motion results in a helical swimming trajectory with pitch p and radius R. (B) Schematics showing the gyration of the cell body. (C) Theoretical model of a zoospore translating in a 2D plane using Resistive Force Theory. (D) The dependence of translational speed UX on the type-1 mastigoneme density (Nm). The range of Nm with symbol (⋆) indicates the values measured by TEM. (E) The effects of beating frequencies of the two flagella, f1 and f2, on zoospore speed UX, (F) power consumption of each flagellum Pk, (G) total power consumption of two flagella (P1+P2), (H) power distributed to the anterior flagellum and (I) propelling efficiency of both flagella η. In these plots, Nm is set at 13 μ⁢m-1.

Figure 4.
Figure 4.. Active turning of individual P. parasitica zoospores in water.

(A) Images of a zoospore changing direction. The two flagella cooperate to help the cell body rotate and steer to a new direction achieving a turning angle Δ⁢θ. (B) Trajectory of the zoospore during the turning event. Three red arrows represent 3 back and forth stroke-like motions. (C) The speed U of the zoospore during the turning event. The turning starts when the speed begins to fluctuate with large magnitude and lower frequency, and lasts for a duration of τs with a rotation of the cell body followed by steering to the new direction. (D) The moving directions θ and the body orientation ψ of the zoospore during the turning event. (E) Images of the anterior flagellum of a zoospore beats with power and recovery stroke, similar to C. reinhardtii’s in a temporal zoom corresponding to the "Rotate" step of the turning event (but not from the same video as (A)). (F) Schematic to describe the gait of the flagella during a turning event. (1-2) Power stroke 1, (2-3) recovery stroke 1, (3-4) power stroke 2.

Appendix 1—figure 1.
Appendix 1—figure 1.. Strategy to apply kymograph to obtain characteristics of beating zoospore flagella.
Appendix 2—figure 1.
Appendix 2—figure 1.. Estimation of τr, τs and Δθ for different variation of Uth.

(A) τr, τs and (B) Δ⁢θ for Uth-10% (C), τr τs and (D) Δ⁢θ for Uth+10%.

Appendix 4—figure 1.
Appendix 4—figure 1.. Strategy to estimate mastigoneme density.

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