Abstract
In a multitude of life's processes, cilia and flagella are found indispensable. Recently, the biflagellated chlorophyte alga Chlamydomonas has become a model organism for the study of ciliary motility and synchronization. Here, we use high-speed, high-resolution imaging of single pipette-held cells to quantify the rich dynamics exhibited by their flagella. Underlying this variability in behaviour are biological dissimilarities between the two flagella—termed cis and trans, with respect to a unique eyespot. With emphasis on the wild-type, we derive limit cycles and phase parametrizations for self-sustained flagellar oscillations from digitally tracked flagellar waveforms. Characterizing interflagellar phase synchrony via a simple model of coupled oscillators with noise, we find that during the canonical swimming breaststroke the cis flagellum is consistently phase-lagged relative to, while remaining robustly phase-locked with, the trans flagellum. Transient loss of synchrony, or phase slippage, may be triggered stochastically, in which the trans flagellum transitions to a second mode of beating with attenuated beat envelope and increased frequency. Further, exploiting this alga's ability for flagellar regeneration, we mechanically induced removal of one or the other flagellum of the same cell to reveal a striking disparity between the beatings of the cis and trans flagella, in isolation. These results are evaluated in the context of the dynamic coordination of Chlamydomonas flagella.
Highlights
Periodicity permeates Nature and its myriad life forms
Just as marching soldiers and Olympic hurdlers alike can have preferential footedness, we find that Chlamydomonas is no exception; resolving within each cycle of its characteristic BS gait we see that one flagellum is consistently phase-lagged with respect to the other
As further indication that Chlamydomonas cells are highly sensitive to fluctuating biochemical cues, we find that the tendency for the two flagella of a given cell to experience phase slips exhibits much greater variation across the population
Summary
Periodicity permeates Nature and its myriad life forms. Oscillatory motions lie at the heart of many important biological and physiological processes, spanning a vast dynamic range of spatial and temporal scales. The striking, periodic flagellar beats of one particular organism shall dictate the following discussion: Chlamydomonas reinhardtii is a unicellular alga whose twin flagella undergo bilateral beating to elicit breaststroke (BS) swimming. For these micrometre-sized cells, their motile appendages, termed flagella, are active filaments that are actuated by internal molecular motor proteins. Metachronously, multitudes of these cilia drive extracellular fluid flows which mediate mucociliary clearance These motile cilia, and their non-motile counterparts, are regulated by complex biochemical networks to perform highly specific functions [14,15]. Mice experiments in which nodal flows are artificially disrupted directly link mechanical flows to positioning of morphogens, which in turn trigger laterality signalling cascades [18]
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