Coordinated beating of algal flagella is mediated by basal coupling

Abstract

Cilia and flagella often exhibit synchronized behavior; this includes phase locking, as seen in Chlamydomonas, and metachronal wave formation in the respiratory cilia of higher organisms. Since the observations by Gray and Rothschild of phase synchrony of nearby swimming spermatozoa, it has been a working hypothesis that synchrony arises from hydrodynamic interactions between beating filaments. Recent work on the dynamics of physically separated pairs of flagella isolated from the multicellular alga Volvox has shown that hydrodynamic coupling alone is sufficient to produce synchrony. However, the situation is more complex in unicellular organisms bearing few flagella. We show that flagella of Chlamydomonas mutants deficient in filamentary connections between basal bodies display markedly different synchronization from the wild type. We perform micromanipulation on configurations of flagella and conclude that a mechanism, internal to the cell, must provide an additional flagellar coupling. In naturally occurring species with 4, 8, or even 16 flagella, we find diverse symmetries of basal body positioning and of the flagellar apparatus that are coincident with specific gaits of flagellar actuation, suggesting that it is a competition between intracellular coupling and hydrodynamic interactions that ultimately determines the precise form of flagellar coordination in unicellular algae.

Batchelor Prize Lecture Fluid dynamics at the scale of the cell

“…The study by Quaranta, Aubin-Tam & Tam (2015) showed no evidence of synchrony in these mutants. A more extensive examination (Wan & Goldstein 2016) showed that when the flagella of these mutants are close enough together for strong hydrodynamic interactions then synchrony is observed, with the symmetries found in the measurements of separated Volvox somatic cells described above. Moreover, nature has provided us with not only biflagellates, but unicellular quadri-, octo-and even hexadecaflagellates, all with known and often elaborate networks of filamentary In each panel, the coloured bars depict time series of beat phases.…”

“…Moreover, nature has provided us with not only biflagellates, but unicellular quadri-, octo-and even hexadecaflagellates, all with known and often elaborate networks of filamentary In each panel, the coloured bars depict time series of beat phases. Reproduced from Wan & Goldstein (2016).…”

“…Systematic study (Wan & Goldstein 2016) of the beating patterns of these organisms show that often the symmetries of the BB connections are mirrored in the patterns of flagellar actuation. An example is shown in figure 14 in the case of quadriflagellates.…”

Hydrodynamic synchronization of flagellar oscillators

“…Which of the different mechanisms dominates in different biological systems will have to determined by future research. Open questions relate in particular to the role of elastic anchorage of the flagellar apparatus [37,73], and the waveform compliance of the flagellar beat [34]. It is not known, which features of the flagellar beat patterns determine whether in-phase or anti-phase synchronization will be stable, as observed e.g.…”

Role of spatial heterogeneity in the collective dynamics of cilia beating in a minimal one-dimensional model

“…This type of large scale coordinated beating pattern is of great importance for efficient propulsion [8][9][10][11][12]. It is now well established that hydrodynamic interactions play a crucial role [7,10,13,14] for the emergence of such large scale metachronal waves.…”