The reaction-diffusion basis of animated patterns in eukaryotic flagella

Cass, James F.; Bloomfield-Gadêlha, Hermes

doi:10.1101/2023.05.26.542447

Cited by 3 publications

(2 citation statements)

References 80 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The greater than expected restrictive force on filament movement is no longer generally thought to be caused just by the drag of negatively strained motors [28]. Instead it is attributed to protein friction in the filaments - the close proximity of proteins is thought to constrain motor protein speed [42], as well as friction intrinsic to the moving components of the motor itself [43, 44].…”

Section: Discussionmentioning

confidence: 99%

A discontinuously coupled network of phase oscillators replicate actomyosin cooperation

Warmington,

Rossiter,

Bloomfield-Gadêlha

2023

Preprint

Self Cite

View full text Add to dashboard Cite

Groups of non-processive myosin motors exhibit complex and non-linear behaviors when binding to actin, operating at larger scales and time frames than individual myosin-head actions. This indicates the presence of strong cooperative disposition, generally attributed to the motor’s biochemistry. Limits in contemporary microscopy prevent verification of motor-filament (un)binding dynamics, whilst mathematical models rely on continuum abstractions in which cooperativity is implicit and individual motor behavior is lacking. Understanding the fundamental interactions driving the emergent behaviour in actomyosin remains an open question. Here we show that the diversity of empirically observedin-vitrooscillations can be explained by a single minimal synchronization model of self-organised time-variable network of Kuramoto oscillators orchestrated by the actomyosin geometry. The synchronization model mirrors the irregular and regular saw-tooth oscillations present inin-vitroactomyosin and sarcomeric contraction experiments, without parameter adjustments, and despite the model’s simplicity. Actomyosin-like behaviour thus arise as a generic property of the discontinuous mechanical coupling in an incommensurate architecture, rather than specific to molecular motor reaction kinetics. This demonstrates that non-biological motors can cooperate similarly to biological motors when working within an actomyosin geometry. This suggests that the actomyosin complex may not depend on motor-specific qualities to achieve its biological function. We build a physical experimental replica with non-biological motors and demonstrate that the brief self-organised connectivity dynamics is sufficient to cause the formation of spontaneous metachronal travelling waves. Global entrainment occurs via spatiotemporal patterning of the connectivity among nodes, coupling a maximum of 35% of motors, whilst minimising velocity changes, in a demonstration of morphological control and self-gearing mechanism. Altogether, the synchronization model reduces mathematical complexity and unify theoretical predictions of observed emergent behaviour. These findings also offer novel insights into synchronizing time-variable networks and potential applications in emulating actomyosin-like behaviors within contemporary robotics using non-biological motors.

show abstract

Section: Discussionmentioning

confidence: 99%

A discontinuously coupled network of phase oscillators replicate actomyosin cooperation

Warmington,

Rossiter,

Bloomfield-Gadêlha

2023

Preprint

Self Cite

View full text Add to dashboard Cite

show abstract

“…But how is the activity of dyneins controlled? The precise mechanism of motor coordination driving the axonemal beat remains a matter of debate [48][49][50][51][52][53][54][55][56] . Almost all theoretical models assume that motor activity is regulated by mechanical deformations such as curvature, sliding or DMT spacing.…”

Section: Mechanisms Of Motor Controlmentioning

confidence: 99%

Twist - torsion coupling in beating axonemes

Striegler,

Friedrich,

Diez

et al. 2024

Preprint

View full text Add to dashboard Cite

Motile cilia and flagella are ubiquitous cell appendages whose regular bending waves pump fluids across tissue surfaces and enable single-cell navigation. Key to these functions are their non-planar waveforms with characteristic torsion. It is not known how torsion, a purely geometric property of the shape, is related to mechanical deformations of the axoneme, the conserved cytoskeletal core of cilia and flagella. Here, we assess torsion and twist in reactivated axonemes isolated from the green alga Chlamydomonas reinhardtii. Using defocused darkfield microscopy and beat-cycle averaging, we resolve the 3D shapes of the axonemal waveform with nanometer precision at millisecond timescales. Our measurements reveal regular hetero-chiral torsion waves propagating base to tip with a peak-to-peak amplitude of 22 °/μm. To investigate if the observed torsion results from axonemal twist, we attach gold nanoparticles to axonemes to measure its cross-section rotation during beating. We find that locally, the axonemal cross-section co-rotates with the bending plane. This co-rotation presents the first experimental evidence for twist-torsion coupling and indicates that twist waves propagate along the axoneme during beating. Our work thus links shape to mechanical deformation of beating axonemes, informing models of motor regulation that shape the beat of motile cilia.

show abstract

Swimming by spinning: spinning-top type rotations regularize sperm swimming into persistently symmetric paths in 3D

Ren

Bloomfield-Gadêlha

2023

Preprint

Self Cite

View full text Add to dashboard Cite

Sperm modulate their flagellar symmetry to navigate through complex physico-chemical environments and achieve reproductive function. Yet it remains elusive how sperm swim forwards despite the inherent asymmetry of several components that constitutes the flagellar engine. Despite the critical importance of symmetry, or the lack of it, on sperm navigation and its physiological state, there is no methodology to date that can robustly detect the symmetry state of the beat in free-swimming sperm in 3D. How does symmetric progressive swimming emerge even for asymmetric beating, and how can beating (a)symmetry be inferred experimentally? Here, we numerically resolve the fluid mechanics of swimming around asymmetrically beating spermatozoa. This reveals that sperm spinning critically regularizes swimming into persistently symmetric paths in 3D, allowing sperm to swim forwards despite any imperfections on the beat. The sperm orientation in three-dimensions, and not the swimming path, can inform the symmetry state of the beat, eliminating the need of tracking the flagellum in 3D. We report a surprising correspondence between the movement of sperm and spinning-top experiments, indicating that the flagellum drives ''spinning-top'' type rotations during sperm swimming, and that this parallel is not a mere analogy. These results may prove essential in future studies on the role of (a)symmetry in spinning and swimming microorganisms and micro-robots, as body orientation detection has been vastly overlooked in favour of swimming path detection. Altogether, sperm rotation may provide a foolproof mechanism for forward propulsion and navigation in nature that would otherwise not be possible for flagella with broken symmetry.

show abstract

The reaction-diffusion basis of animated patterns in eukaryotic flagella

Cited by 3 publications

References 80 publications

A discontinuously coupled network of phase oscillators replicate actomyosin cooperation

A discontinuously coupled network of phase oscillators replicate actomyosin cooperation

Twist - torsion coupling in beating axonemes

Swimming by spinning: spinning-top type rotations regularize sperm swimming into persistently symmetric paths in 3D

Contact Info

Product

Resources

About