skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Intracellular coupling modulates biflagellar synchrony
Beating flagella exhibit a variety of synchronization modes. This synchrony has long been attributed to hydrodynamic coupling between the flagella. However, recent work with flagellated algae indicates that a mechanism internal to the cell, through the contractile fibres connecting the flagella basal bodies, must be at play to actively modulate flagellar synchrony. Exactly how basal coupling mediates flagellar coordination remains unclear. Here, we examine the role of basal coupling in the synchronization of the model biflagellate Chlamydomonas reinhardtii using a series of mathematical models of decreasing levels of complexity. We report that basal coupling is sufficient to achieve inphase, antiphase and bistable synchrony, even in the absence of hydrodynamic coupling and flagellar compliance. These modes can be reached by modulating the activity level of the individual flagella or the strength of the basal coupling. We observe a slip mode when allowing for differential flagellar activity, just as in experiments with live cells. We introduce a dimensionless ratio of flagellar activity to basal coupling that is predictive of the mode of synchrony. This ratio allows us to query biological parameters which are not yet directly measurable experimentally. Our work shows a concrete route for cells to actively control the synchronization of their flagella.  more » « less
Award ID(s):
2100209
PAR ID:
10327498
Author(s) / Creator(s):
; ; ;
Date Published:
Journal Name:
Journal of The Royal Society Interface
Volume:
18
Issue:
174
ISSN:
1742-5689
Page Range / eLocation ID:
20200660
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. We present a mathematical model of lophotrichous bacteria, motivated by Pseudomonas putida, which swim through fluid by rotating a cluster of multiple flagella extended from near one pole of the cell body. Although the flagella rotate individually, they are typically bundled together, enabling the bacterium to exhibit three primary modes of motility: push, pull, and wrapping. One key determinant of these modes is the coordination between motor torque and rotational direction of motors. The computational variations in this coordination reveal a wide spectrum of dynamical motion regimes, which are modulated by hydrodynamic interactions between flagellar filaments. These dynamic modes can be categorized into two groups based on the collective behavior of flagella, i.e., bundled and unbundled configurations. For some of these configurations, experimental examples from fluorescence microscopy recordings of swimming P. putida cells are also presented. Furthermore, we analyze the characteristics of stable bundles, such as push and pull, and investigate the dependence of swimming behaviors on the elastic properties of the flagella. 
    more » « less
  2. To swim through a viscous fluid, a flagellated bacterium must overcome the fluid drag on its body by rotating a flagellum or a bundle of multiple flagella. Because the drag increases with the size of bacteria, it is expected theoretically that the swimming speed of a bacterium inversely correlates with its body length. Nevertheless, despite extensive research, the fundamental size–speed relation of flagellated bacteria remains unclear with different experiments reporting conflicting results. Here, by critically reviewing the existing evidence and synergizing our own experiments of large sample sizes, hydrodynamic modeling, and simulations, we demonstrate that the average swimming speed ofEscherichia coli, a premier model of peritrichous bacteria, is independent of their body length. Our quantitative analysis shows that such a counterintuitive relation is the consequence of the collective flagellar dynamics dictated by the linear correlation between the body length and the number of flagella of bacteria. Notably, our study reveals how bacteria utilize the increasing number of flagella to regulate the flagellar motor load. The collective load sharing among multiple flagella results in a lower load on each flagellar motor and therefore faster flagellar rotation, which compensates for the higher fluid drag on the longer bodies of bacteria. Without this balancing mechanism, the swimming speed of monotrichous bacteria generically decreases with increasing body length, a feature limiting the size variation of the bacteria. Altogether, our study resolves a long-standing controversy over the size–speed relation of flagellated bacteria and provides insights into the functional benefit of multiflagellarity in bacteria. 
    more » « less
  3. Discher, Dennis (Ed.)
    Hydrodynamic flow produced by multiciliated cells is critical for fluid circulation and cell motility. Hundreds of cilia beat with metachronal synchrony for fluid flow. Cilia-driven fluid flow produces extracellular hydrodynamic forces that cause neighboring cilia to beat in a synchronized manner. However, hydrodynamic coupling between neighboring cilia is not the sole mechanism that drives cilia synchrony. Cilia are nucleated by basal bodies (BBs) that link to each other and to the cell’s cortex via BB-associated appendages. The intracellular BB and cortical network is hypothesized to synchronize ciliary beating by transmitting cilia coordination cues. The extent of intracellular ciliary connections and the nature of these stimuli remain unclear. Moreover, how BB connections influence the dynamics of individual cilia has not been established. We show by focused ion beam scanning electron microscopy imaging that cilia are coupled both longitudinally and laterally in the ciliate Tetrahymena thermophila by the underlying BB and cortical cytoskeletal network. To visualize the behavior of individual cilia in live, immobilized Tetrahymena cells, we developed Delivered Iron Particle Ubiety Live Light (DIPULL) microscopy. Quantitative and computer analyses of ciliary dynamics reveal that BB connections control ciliary waveform and coordinate ciliary beating. Loss of BB connections reduces cilia-dependent fluid flow forces. 
    more » « less
  4. Abstract Lophotrichous bacteria swim through fluid by rotating their flagellar bundle extended collectively from one pole of the cell body. Cells experience modes of motility such as push, pull, and wrapping, accompanied by pauses of motor rotation in between. We present a mathematical model of a lophotrichous bacterium and investigate the hydrodynamic interaction of cells to understand their swimming mechanism. We classify the swimming modes which vary depending on the bending modulus of the hook and the magnitude of applied torques on the motor. Given the hook’s bending modulus, we find that there exist corresponding critical thresholds of the magnitude of applied torques that separate wrapping from pull in CW motor rotation, and overwhirling from push in CCW motor rotation, respectively. We also investigate reoriented directions of cells in three-dimensional perspectives as the cell experiences different series of swimming modes. Our simulations show that the transition from a wrapping mode to a push mode and pauses in between are key factors to determine a new path and that the reoriented direction depends upon the start time and duration of the pauses. It is also shown that the wrapping mode may help a cell to escape from the region where the cell is trapped near a wall. 
    more » « less
  5. null (Ed.)
    Combustion instability, which is the result of a coupling between combustor acoustic modes and unsteady flame heat release rate, is a severely limiting factor in the operability and performance of modern gas turbine engines. This coupling can occur through different coupling pathways, such as flow field fluctuations or equivalence ratio fluctuations. In realistic combustor systems, there are complex hydrodynamic and thermo-chemical processes involved, which can lead to multiple coupling pathways. In order to understand and predict the mechanisms that govern the onset of combustion instability in real gas turbine engines, we consider the influences that each of these coupling pathways can have on the stability and dynamics of a partially-premixed, swirl-stabilized flame. In this study, we use a model gas turbine combustor with two concentric swirling nozzles of air, separated by a ring of fuel injectors, operating at an elevated pressure of 5 bar. The flow split between the two streams is systematically varied to observe the impact on the flow and flame dynamics. High-speed stereoscopic particle image velocimetry, OH planar laser-induced fluorescence, and acetone planar laser-induced fluorescence are used to obtain information about the velocity field, flame, and fuel-flow behavior, respectively. Depending on the flow conditions, a thermoacoustic oscillation mode or a hydrodynamic mode, identified as the precessing vortex core, is present. The focus of this study is to characterize the mixture coupling processes in this partially-premixed flame as well as the impact that the velocity oscillations have on mixture coupling. Our results show that, for this combustor system, changing the flow split between the two concentric nozzles can alter the dominant harmonic oscillation modes in the system, which can significantly impact the dispersion of fuel into air, thereby modulating the local equivalence ratio of the flame. This insight can be used to design instability control mechanisms in real gas turbine engines. 
    more » « less