Control of helical navigation by three-dimensional flagellar beating

Cortese, Dario; Wan, Kirsty Y.

doi:10.1101/2020.09.27.315606

Cited by 9 publications

(9 citation statements)

References 52 publications

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“…In all three cases, cells swim smoothly flagella-first (puller-type) at speeds of 𝒪 (100) µ m /s . The translational motion is coupled to an axial rotation to produce swimming along helical trajectories [41]. Abrupt gait transitions can occur either spontaneously or when triggered by mechanical contact, during which the flagella are directed to the front of the cell in a so-called shock-response [42].…”

Section: Resultsmentioning

confidence: 99%

A minimal robophysical model of quadriflagellate self-propulsion

Diaz

Robinson

Ozkan-Aydin

et al. 2021

Preprint

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Locomotion 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=0.1-0.5). 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, with parallel appendage placement consistently leading to slower propulsion. By creating a minimal robot that can successfully reproduce cilia-inspired drag-based swimmging, our work paves the way for the design of next-generation devices that have the capacity to autonomously navigate aqueous environments.

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Section: Resultsmentioning

confidence: 99%

A minimal robophysical model of quadriflagellate self-propulsion

Diaz

Robinson

Ozkan-Aydin

et al. 2021

Preprint

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“…Here cells rotating around an axis can maintain stable helical swimming. Periodic stroke patterns produce superhelical trajectories over long times [ 339 ]. Cells detect gradients perpendicular to the helix axis and gradually steer toward gradients by adjusting the alignment between the swimming direction and gradient (error correction).…”

Section: Cellular and Biophysical Innovations Underpinning Eukaryoticmentioning

confidence: 99%

Origins of eukaryotic excitability

Wan

Jékely

2021

Phil. Trans. R. Soc. B

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All living cells interact dynamically with a constantly changing world. Eukaryotes, in particular, evolved radically new ways to sense and react to their environment. These advances enabled new and more complex forms of cellular behaviour in eukaryotes, including directional movement, active feeding, mating, and responses to predation. But what are the key events and innovations during eukaryogenesis that made all of this possible? Here we describe the ancestral repertoire of eukaryotic excitability and discuss five major cellular innovations that enabled its evolutionary origin. The innovations include a vastly expanded repertoire of ion channels, the emergence of cilia and pseudopodia, endomembranes as intracellular capacitors, a flexible plasma membrane and the relocation of chemiosmotic ATP synthesis to mitochondria, which liberated the plasma membrane for more complex electrical signalling involved in sensing and reacting. We conjecture that together with an increase in cell size, these new forms of excitability greatly amplified the degrees of freedom associated with cellular responses, allowing eukaryotes to vastly outperform prokaryotes in terms of both speed and accuracy. This comprehensive new perspective on the evolution of excitability enriches our view of eukaryogenesis and emphasizes behaviour and sensing as major contributors to the success of eukaryotes. This article is part of the theme issue ‘Basal cognition: conceptual tools and the view from the single cell’.

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“…To capture this effect and, more generally, to represent adequately the signature on the generated flow left by flagella and cilia that do not beat in a single plane, more complex systems of singularities would be needed. We hope that our study may motivate also others to investigate the question of which systems of singularities may be effective in coarse-graining the flows associated with the three-dimensional trajectories that have attracted interest in the recent bio-physical literature on microswimmers [3,8,13,[24][25][26][27][28].…”

Section: Discussionmentioning

confidence: 99%

“…The technical challenges involved have prevented this, at least until now. In fact, extending to three dimensions the two-dimensional results on trajectories and flows obtained in recent years is one of the frontiers in the research on the biophysics of microswimmers, as witnessed by the increasing focus on three-dimensional effects in the recent literature [8,13,[24][25][26][27][28].…”

Section: Introductionmentioning

confidence: 99%

HowEuglena gracilisswims: Flow field reconstruction and analysis

et al. 2021

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Euglena gracilis is a unicellular organism that swims by beating a single anterior flagellum. We study the nonplanar waveforms spanned by the flagellum during a swimming stroke and the three-dimensional flows that they generate in the surrounding fluid. Starting from a small set of time-indexed images obtained by optical microscopy on a swimming Euglena cell, we construct a numerical interpolation of the stroke. We define an optimal interpolation (which we call synthetic stroke) by minimizing the discrepancy between experimentally measured velocities (of the swimmer) and those computed by solving numerically the equations of motion of the swimmer driven by the trial interpolated stroke. The good match we obtain between experimentally measured and numerically computed trajectories provides a first validation of our synthetic stroke. We further validate the procedure by studying the flow velocities induced in the surrounding fluid. We compare the experimentally measured flow fields with the corresponding quantities computed by solving numerically the Stokes equations for the fluid flow, in which the forcing is provided by the synthetic stroke, and find good matching. Finally, we use the synthetic stroke to derive a coarse-grained model of the flow field resolved in terms of a few dominant singularities. The far field is well approximated by a time-varying Stresslet, and we show that the average behavior of Euglena during one stroke is that of an off-axis puller. The reconstruction of the flow field closer to the swimmer body requires a more complex system of singularities. A system of two Stokeslets and one Rotlet, that can be loosely associated with the force exerted by the flagellum, the drag of the body, and a torque to guarantee rotational equilibrium, provides a good approximation.

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Control of helical navigation by three-dimensional flagellar beating

Cited by 9 publications

References 52 publications

A minimal robophysical model of quadriflagellate self-propulsion

A minimal robophysical model of quadriflagellate self-propulsion

Origins of eukaryotic excitability

HowEuglena gracilisswims: Flow field reconstruction and analysis

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