Beat regulation in twisted axonemes

TL;DR

This paper investigates how stresses within the axoneme regulate dynein motor activity to produce coordinated, wave-like flagellar motion, emphasizing the role of twist in generating realistic three-dimensional waveforms.

Contribution

It demonstrates that radial and transverse stress regulation requires axoneme twist for effective coordination, and models emergent three-dimensional beating patterns consistent with biological observations.

Findings

Radial and transverse stresses regulate dynein motors only with twist.

Shear stress regulation can occur without twist.

Twisted axonemes produce non-planar waveforms matching observed flagellar motions.

Abstract

Cilia and flagella are hairlike organelles that propel cells through fluid. The active motion of the axoneme, the motile structure inside cilia and flagella, is powered by molecular motors of the dynein family. These motors generate forces and torques that slide and bend the microtubule doublets within the axoneme. To create regular waveforms the activities of the dyneins must be coordinated. It is thought that coordination is mediated by stresses due to radial, transverse, or sliding deformations, that build up within the moving axoneme. However, which particular component of the stress regulates the motors to produce the observed flagellar waveforms remains an open question. To address this question, we describe the axoneme as a three-dimensional bundle of filaments and characterize its mechanics. We show that regulation of the motors by radial and transverse stresses can lead to a coordinated flagellar motion only in the presence of twist. By comparison, regulation by shear stress is possible without twist. We calculate emergent beating patterns in twisted axonemes resulting from regulation by transverse stresses. The waveforms are similar to those observed in flagella of Chlamydomonas and sperm. Due to the twist, the waveform has non-planar components, which result in swimming trajectories such as twisted ribbons and helices that agree with observations.