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Abstract It remains unclear how flagella generate propulsive, oscillatory waveforms. While it is well known that dynein motors, in combination with passive cytoskeletal elements, drive the bending of the axoneme by applying shearing forces and bending moments to microtubule doublets, the origin of rhythmicity is still mysterious. Most conceptual models of flagellar oscillation involve dynein regulation or switching, so that dynein activity first on one side of the axoneme, then the other, drives bending. In contrast, a “viscoelastic flutter” mechanism has recently been proposed, based on a dynamic structural instability. Simple mathematical models of coupled elastic beams in viscous fluid, subjected to steady, axially distributed, dynein forces of sufficient magnitude, can exhibit oscillatory motion without any switching or dynamic regulation. Here we introduce more realistic finite element (FE) models of 6‐doublet and 9‐doublet flagella, with radial spokes and interdoublet links that slide along the central pair or corresponding doublet. These models demonstrate the viscoelastic flutter mechanism. Above a critical force threshold, these models exhibit an abrupt onset of propulsive, wavelike oscillations typical of flutter instability. Changes in the magnitude and spatial distribution of steady dynein force, or to viscous resistance, lead to behavior qualitatively consistent with experimental observations. This study demonstrates the ability of FE models to simulate nonlinear interactions between axonemal components during flagellar beating, and supports the plausibility of viscoelastic flutter as a mechanism of flagellar oscillation.
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Self-sustained three-dimensional beating of a model eukaryotic flagellum
Flagella and cilia are common features of a wide variety of biological cells and play important roles in locomotion and feeding at the microscale. The beating of flagella is controlled by molecular motors that exert forces along the length of the flagellum and are regulated by a feedback mechanism coupled to the flagella deformation. We develop a three-dimensional (3D) flagellum beating model based on sliding-controlled motor feedback, accounting for both bending and twist, as well as differential bending resistances along and orthogonal to the major bending plane of the flagellum. We show that beating is generated and sustained spontaneously for a sufficiently high motor activity through an instability mechanism. Isotropic bending rigidities in the flagellum lead to 3D helical beating patterns. By contrast, anisotropic flagella present a rich variety of wave-like beating dynamics, including both 3D beating patterns as well as planar beating patterns. We show that the ability to generate nearly planar beating despite the 3D beating machinery requires only a modest degree of bending anisotropy, and is a feature observed in many eukaryotic flagella such as mammalian spermatozoa.
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- Award ID(s):
- 2215705
- PAR ID:
- 10464592
- Date Published:
- Journal Name:
- Soft Matter
- Volume:
- 18
- Issue:
- 28
- ISSN:
- 1744-683X
- Page Range / eLocation ID:
- 5312 to 5322
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1039/D2SM00514J
