scholarly journals A minimal robophysical model of quadriflagellate self-propulsion

2021 ◽  
Author(s):  
Kelimar Diaz ◽  
Tommie L. Robinson ◽  
Yasemin Ozkan Aydin ◽  
Enes Aydin ◽  
Daniel I. Goldman ◽  
...  
Keyword(s):  
Central Body ◽  
Swimming Performance ◽  
M Cell ◽  
Trot Gait ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Aqueous Environments ◽  
Cilia And Flagella ◽  
Microalgal Species ◽  
Phase Relationships

AbstractLocomotion at the microscale is remarkably sophisticated. Microorganisms have evolved diverse strategies to move within highly viscous environments, using deformable, propulsion-generating appendages such as cilia and flagella to drive helical or undulatory motion. In single-celled algae, these appendages can be arranged in different ways around an approximately 10µm cell body, and coordinated in distinct temporal patterns. Inspired by the observation that some quadriflagellates (bearing four flagella) have an outwardly similar morphology and flagellar beat pattern, yet swim at different speeds, this study seeks to determine whether variations in swimming performance could arise solely from differences in swimming gait. Robotics approaches are particularly suited to such investigations, where the phase relationships between appendages can be readily manipulated. Here, we developed autonomous, algae-inspired robophysical models that can self-propel in a viscous fluid. These macroscopic robots (length and width = 8.5 cm, height = 2 cm) have four independently actuated ‘flagella’ that oscillate back and forth under low-Reynolds number conditions (Re∼ 𝒪(10−1)). We tested the swimming performance of these robot models with appendages arranged in one of two distinct configurations, and coordinated in one of three distinct gaits. The gaits, namely the pronk, the trot, and the gallop, correspond to gaits adopted by distinct microalgal species. When the appendages are inserted perpendicularly around a central ‘body’, the robot achieved a net performance of 0.15−0.63 body lengths per cycle, with the trot gait being the fastest. Robotic swimming performance was found to be comparable to that of the algal microswimmers across all gaits. By creating a minimal robot that can successfully reproduce cilia-inspired drag-based swimming, our work paves the way for the design of next-generation devices that have the capacity to autonomously navigate aqueous environments.

scholarly journals Tubulin glycylation controls axonemal dynein activity, flagellar beat, and male fertility

Science ◽  
2021 ◽  
Vol 371 (6525) ◽  
pp. eabd4914
Author(s):  
Sudarshan Gadadhar ◽  
Gonzalo Alvarez Viar ◽  
Jan Niklas Hansen ◽  
An Gong ◽  
Aleksandr Kostarev ◽  
...  
Keyword(s):  
Posttranslational Modifications ◽  
Male Fertility ◽  
Electron Tomography ◽  
Structural Basis ◽  
Cellular Functions ◽  
Flagellar Beat ◽  
Cryo Electron Tomography ◽  
Axonemal Dynein ◽  
Dynein Arms ◽  
Cilia And Flagella

Posttranslational modifications of the microtubule cytoskeleton have emerged as key regulators of cellular functions, and their perturbations have been linked to a growing number of human pathologies. Tubulin glycylation modifies microtubules specifically in cilia and flagella, but its functional and mechanistic roles remain unclear. In this study, we generated a mouse model entirely lacking tubulin glycylation. Male mice were subfertile owing to aberrant beat patterns of their sperm flagella, which impeded the straight swimming of sperm cells. Using cryo–electron tomography, we showed that lack of glycylation caused abnormal conformations of the dynein arms within sperm axonemes, providing the structural basis for the observed dysfunction. Our findings reveal the importance of microtubule glycylation for controlled flagellar beating, directional sperm swimming, and male fertility.

Analysis of the Flagellar Beat Pattern of Male Ectocarpus Siliculosus Gametes (Phaeophyta) in Relation to Chemotactic Stimulation by Female Cells

1981 ◽  
Vol 92 (1) ◽  
pp. 53-66
Author(s):  
ANNETTE GELLER ◽  
DIETER G. MÜLLER
Keyword(s):  
Linear Correlation ◽  
Mode Of Action ◽  
High Speed ◽  
Sex Attractant ◽  
Cell Axis ◽  
Ectocarpus Siliculosus ◽  
Bending Waves ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Negative Linear Correlation

Heterocontic male Ectocarpus siliculosus gametes respond to the sex-attractant ectocarpen by changing their locomotive behaviour. However, the mode of action of the flagella is not changed by the presence of ectocarpen. High-speed cinemicrography shows that gametes moving close to a coverglass perform planar bending waves with their front flagellum. Straight or slightly curved swimming paths are generated by enhanced upward bends of the front flagellum to compensate for the asymmetrical insertion of both flagella. Narrower curves are connected with increasing downward bends of the front flagellum. There is a negative linear correlation between the average deflexion of the front flagellum (μm) from the cell axis and the radius of track (correlation coefficient 0.94). Additionally, freely swimming gametes exhibit elliptical and rotary wave motions, suggesting a relationship between thigmotaxis and mode of action of the front flagellum. The rigid hind flagellum performs one rapid sideward beat when the gametes swim in narrow curves. This appears to provide a steering function.

scholarly journals Targeted inactivation of the mouse epididymal beta-defensin 41 alters sperm flagellar beat pattern and zona pellucida binding

2016 ◽  
Vol 427 ◽  
pp. 143-154 ◽  
Author(s):  
Ida Björkgren ◽  
Luis Alvarez ◽  
Nelli Blank ◽  
Melanie Balbach ◽  
Heikki Turunen ◽  
...  
Keyword(s):  
Zona Pellucida ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Targeted Inactivation

scholarly journals Time-reversal symmetric component of the flagellar beat enhances the translational and rotational velocities of isolated Chlamydomonas flagella

2021 ◽  
Author(s):  
Azam Gholami ◽  
Raheel Ahmad ◽  
Albert J Bae ◽  
Alain Pumir ◽  
Eberhard Bodenschatz
Keyword(s):  
Beat Frequency ◽  
Fluid Flows ◽  
Symmetric Mode ◽  
Wave Component ◽  
Intrinsic Curvature ◽  
Flagellar Beat ◽  
Cilia And Flagella ◽  
Micro Organisms ◽  
Insight Into ◽  
Dynamic Wave

The beating of cilia and flagella is essential to perform many important biological functions, including generating fluid flows on the cell surface or propulsion of micro-organisms. In this work, we analyze the motion of isolated and demembranated flagella from green algae Chlamydomonas reinhardtii, which act as ATP-driven micro-swimmers. The waveform of the Chlamydomonas beating flagella has an asymmetric waveform that is known to involve the superposition of a static component, corresponding to a fixed, intrinsic curvature, and a dynamic wave component traveling in the base-to-tip direction at the fundamental beat frequency, plus higher harmonics. Here, we demonstrate that these modes are not sufficient to reproduce the observed flagella waveforms. We find that two extra modes play an essential role to describe the motion: first, a time-symmetric mode, which corresponds to a global oscillation of the axonemal curvature, and second, a secondary tip-to-base wave component at the fundamental frequency that propagates opposite to the dominant base-to-tip wave, albeit with a smaller amplitude. Although the time-symmetric mode cannot, by itself, contribute to propulsion (scallop theorem), it does enhance the translational and rotational velocities of the flagellum by approximately a factor of 2. This mode highlights a long-range coupled on/off activity of force-generating dynein motors and can provide further insight into the underling biology of the ciliary beat.

scholarly journals Reconstruction of the three-dimensional beat pattern underlying swimming behaviors of sperm

2021 ◽  
Vol 44 (7) ◽  
Author(s):  
A. Gong ◽  
S. Rode ◽  
G. Gompper ◽  
U. B. Kaupp ◽  
J. Elgeti ◽  
...  
Keyword(s):  
Three Dimensional ◽  
Intrinsic Property ◽  
Human Sperm ◽  
Bending Waves ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Glass Interface ◽  
Two Space Dimensions ◽  
Swimming Trajectories ◽  
Physical And Chemical

Abstract  The eukaryotic flagellum propels sperm cells and simultaneously detects physical and chemical cues that modulate the waveform of the flagellar beat. Most previous studies have characterized the flagellar beat and swimming trajectories in two space dimensions (2D) at a water/glass interface. Here, using refined holographic imaging methods, we report high-quality recordings of three-dimensional (3D) flagellar bending waves. As predicted by theory, we observed that an asymmetric and planar flagellar beat results in a circular swimming path, whereas a symmetric and non-planar flagellar beat results in a twisted-ribbon swimming path. During swimming in 3D, human sperm flagella exhibit torsion waves characterized by maxima at the low curvature regions of the flagellar wave. We suggest that these torsion waves are common in nature and that they are an intrinsic property of beating axonemes. We discuss how 3D beat patterns result in twisted-ribbon swimming paths. This study provides new insight into the axoneme dynamics, the 3D flagellar beat, and the resulting swimming behavior. Graphic abstract

scholarly journals Control of helical navigation by three-dimensional flagellar beating

2020 ◽  
Author(s):  
Dario Cortese ◽  
Kirsty Y. Wan
Keyword(s):  
High Speed ◽  
Three Dimensional ◽  
Axial Rotation ◽  
Live Cells ◽  
High Speed Imaging ◽  
Flagellar Beat ◽  
Motile Cells ◽  
Beat Pattern ◽  
Swimming Trajectories ◽  
Realistic Geometries

Helical swimming is a ubiquitous strategy for motile cells to generate self-gradients for environmental sensing. The model biflagellate Chlamydomonas reinhardtii rotates at a constant 1 – 2 Hz as it swims, but the mechanism is unclear. Here, we show unequivocally that the rolling motion derives from a persistent, non-planar flagellar beat pattern. This is revealed by high-speed imaging and micromanipulation of live cells. We construct a fully-3D model to relate flagellar beating directly to the free-swimming trajectories. For realistic geometries, the model reproduces both the sense and magnitude of the axial rotation of live cells. We show that helical swimming requires further symmetry-breaking between the two flagella. These functional differences underlie all tactic responses, particularly phototaxis. We propose a control strategy by which cells steer towards or away from light by modulating the sign of biflagellar dominance.

scholarly journals SpermQ–A Simple Analysis Software to Comprehensively Study Flagellar Beating and Sperm Steering

Cells ◽  
2018 ◽  
Vol 8 (1) ◽  
pp. 10 ◽  
Author(s):  
Jan Hansen ◽  
Sebastian Rassmann ◽  
Jan Jikeli ◽  
Dagmar Wachten
Keyword(s):  
Female Genital Tract ◽  
Time Lapse ◽  
Dark Field ◽  
Comprehensive Analysis ◽  
Analysis Software ◽  
Environmental Signals ◽  
Common Time ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Motile Cilia

Motile cilia, also called flagella, are found across a broad range of species; some cilia propel prokaryotes and eukaryotic cells like sperm, while cilia on epithelial surfaces create complex fluid patterns e.g., in the brain or lung. For sperm, the picture has emerged that the flagellum is not only a motor but also a sensor that detects stimuli from the environment, computing the beat pattern according to the sensory input. Thereby, the flagellum navigates sperm through the complex environment in the female genital tract. However, we know very little about how environmental signals change the flagellar beat and, thereby, the swimming behavior of sperm. It has been proposed that distinct signaling domains in the flagellum control the flagellar beat. However, a detailed analysis has been mainly hampered by the fact that current comprehensive analysis approaches rely on complex microscopy and analysis systems. Thus, knowledge on sperm signaling regulating the flagellar beat is based on custom quantification approaches that are limited to only a few aspects of the beat pattern, do not resolve the kinetics of the entire flagellum, rely on manual, qualitative descriptions, and are only a little comparable among each other. Here, we present SpermQ, a ready-to-use and comprehensive analysis software to quantify sperm motility. SpermQ provides a detailed quantification of the flagellar beat based on common time-lapse images acquired by dark-field or epi-fluorescence microscopy, making SpermQ widely applicable. We envision SpermQ becoming a standard tool in flagellar and motile cilia research that allows to readily link studies on individual signaling components in sperm and distinct flagellar beat patterns.

scholarly journals A steering mechanism for phototaxis in Chlamydomonas

2015 ◽  
Vol 12 (104) ◽  
pp. 20141164 ◽  
Author(s):  
Rachel R. Bennett ◽  
Ramin Golestanian
Keyword(s):  
Light Intensity ◽  
Mechanical Model ◽  
Light Signal ◽  
Negative Phototaxis ◽  
Forward Motion ◽  
Flagellar Beat ◽  
Beat Pattern ◽  
Steering Mechanism ◽  
Run And Tumble ◽  
Robust To Noise

Chlamydomonas shows both positive and negative phototaxis. It has a single eyespot near its equator, and as the cell rotates during the forward motion, the light signal received by the eyespot varies. We use a simple mechanical model of Chlamydomonas that couples the flagellar beat pattern to the light intensity at the eyespot to demonstrate a mechanism for phototactic steering that is consistent with observations. The direction of phototaxis is controlled by a parameter in our model, and the steering mechanism is robust to noise. Our model shows switching between directed phototaxis when the light is on and run-and-tumble behaviour in the dark.

scholarly journals Dynamic curvature regulation accounts for the symmetric and asymmetric beats of Chlamydomonas flagella

eLife ◽  
2016 ◽  
Vol 5 ◽  
Author(s):  
Pablo Sartori ◽  
Veikko F Geyer ◽  
Andre Scholich ◽  
Frank Jülicher ◽  
Jonathon Howard
Keyword(s):  
Time Derivative ◽  
Model Systems ◽  
Adaptation Mechanism ◽  
Normal Forces ◽  
Flagellar Beat ◽  
Experimental Approaches ◽  
Cilia And Flagella ◽  
The One ◽  
Proposed Regulation ◽  
Curvature Control

Cilia and flagella are model systems for studying how mechanical forces control morphology. The periodic bending motion of cilia and flagella is thought to arise from mechanical feedback: dynein motors generate sliding forces that bend the flagellum, and bending leads to deformations and stresses, which feed back and regulate the motors. Three alternative feedback mechanisms have been proposed: regulation by the sliding forces, regulation by the curvature of the flagellum, and regulation by the normal forces that deform the cross-section of the flagellum. In this work, we combined theoretical and experimental approaches to show that the curvature control mechanism is the one that accords best with the bending waveforms of Chlamydomonas flagella. We make the surprising prediction that the motors respond to the time derivative of curvature, rather than curvature itself, hinting at an adaptation mechanism controlling the flagellar beat.

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