scholarly journals Coordinated beating of algal flagella is mediated by basal coupling

2016 ◽  
Vol 113 (20) ◽  
pp. E2784-E2793 ◽  
Author(s):  
Kirsty Y. Wan ◽  
Raymond E. Goldstein

Cilia and flagella often exhibit synchronized behavior; this includes phase locking, as seen inChlamydomonas, 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 algaVolvoxhas 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 ofChlamydomonasmutants 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.

2017 ◽  
Vol 836 ◽  
pp. 304-323 ◽  
Author(s):  
Hanliang Guo ◽  
Lisa Fauci ◽  
Michael Shelley ◽  
Eva Kanso

Cilia and flagella are essential building blocks for biological fluid transport and locomotion at the micrometre scale. They often beat in synchrony and may transition between different synchronization modes in the same cell type. Here, we investigate the behaviour of elastic microfilaments, protruding from a surface and driven at their base by a configuration-dependent torque. We consider full hydrodynamic interactions among and within filaments and no slip at the surface. Isolated filaments exhibit periodic deformations, with increasing waviness and frequency as the magnitude of the driving torque increases. Two nearby but independently driven filaments synchronize their beating in-phase or anti-phase. This synchrony arises autonomously via the interplay between hydrodynamic coupling and filament elasticity. Importantly, in-phase and anti-phase synchronization modes are bistable and coexist for a range of driving torques and separation distances. These findings are consistent with experimental observations of in-phase and anti-phase synchronization in pairs of cilia and flagella and could have important implications on understanding the biophysical mechanisms underlying transitions between multiple synchronization modes.


2019 ◽  
Vol 375 (1792) ◽  
pp. 20190393 ◽  
Author(s):  
Kirsty Y. Wan

Living creatures exhibit a remarkable diversity of locomotion mechanisms, evolving structures specialized for interacting with their environment. In the vast majority of cases, locomotor behaviours such as flying, crawling and running are orchestrated by nervous systems. Surprisingly, microorganisms can enact analogous movement gaits for swimming using multiple, fast-moving cellular protrusions called cilia and flagella. Here, I demonstrate intermittency, reversible rhythmogenesis and gait mechanosensitivity in algal flagella, to reveal the active nature of locomotor patterning. In addition to maintaining free-swimming gaits, I show that the algal flagellar apparatus functions as a central pattern generator that encodes the beating of each flagellum in a network in a distinguishable manner. The latter provides a novel symmetry-breaking mechanism for cell reorientation. These findings imply that the capacity to generate and coordinate complex locomotor patterns does not require neural circuitry but rather the minimal ingredients are present in simple unicellular organisms. This article is part of the Theo Murphy meeting issue ‘Unity and diversity of cilia in locomotion and transport’.


During the last five years a small group in this Laboratory has been studying the potentialities of the flagellar apparatus of Chlamydomonas reinhardii for the study of growth and morphopoiesis. The results have been recorded in a number of papers (Randall et al . 1964; Warr et al . 1966; Hookes, Randall & Hopkins 1967; Randall et al . 1967). It is self-evident that the understanding of both growth and morphopoiesis in physical chemical and biological terms will most readily be brought about by the examination of the least complex biological systems, i. e. those that contain the fewest chemical and structural entities and are under the control of a strictly limited number of genes; not for preference a multicellular organism or organ, or even a single cell; but rather a virus or organelle. One would hope by this means to limit the number of genes implicated to something less than 10 2 . An outstanding analysis of the morphopoiesis of T-even bacteriophages has been carried out in recent years by workers in Geneva and Pasadena (see, for example, Kellenberger 1964; Kellenberger & Boy de la Tour 1965; Epstein et al . 1963; Edgar & Wood 1966). In the present investigations the methods and techniques of genetics, of optical and electron microscopy (in conjunction with optical diffraction studies of electron micrographs), radioautography and, to some extent, biochemistry have been used. During the last 15 years the structure of cilia and flagella, their basal bodies and associated cortical structures in various organisms (see, for example Fawcett 1961; Gibbons & Grimstone 1960; Satir 1965; Ringo 1966, 1967; Cavalier-Smith 1967; Allen 1967) have been investigated in some detail. Figure 20, plate 8, illustrates the appearance of the living organism in motion and figure 21 the fine structure of the flagellar apparatus ( FA ) of the alga Chlamydomonas reinhardii , a biflagellate member of the Chlorophyceae. The FA consists essentially of two normally motile flagella F , external to the cell (figure 20) and two internal basal bodies ( BB ). Each basal body is joined to its flagellum by a transition region TR (figure 21). The basal bodies ( BB ) lie in the main diametral plane of the organism and are joined by a fibrous band ( FB ) (figure 21). The external flagellum, bounded by a membrane continuous with the plasma membrane, contains the axoneme and its subsidiary structures. We shall be concerned chiefly with the basic features of the axoneme of the flagellum, i. e. the two central fibrils and the nine outer pairs. Each of these fibrils is apparently tubular in form and generally similar to the microtubules found in many types of cell (e. g. Tilney & Porter 1965; Tilney & Porter 1967; Peters & Vaughin 1967; Hepler & Newcomb 1964). The appearance in the electron microscope of an intact fragment of tubule (outer pair) from a disrupted negatively stained flagellum of C. reinhardii is shown in figure 24 a , plate 9. The structural interpretation of micrographs of flagellar tubules has been discussed by Grimstone & Klug (1966) and Hookes, Randall & Hopkins (1967) and will be referred to subsequently. For fuller details of the fine structure of the FA of C. reinhardii , as a whole, reference should be made to Ringo (1966; 1967) and to Cavalier-Smith (1967).


1967 ◽  
Vol 33 (3) ◽  
pp. 543-571 ◽  
Author(s):  
David L. Ringo

The biflagellate alga Chlamydomonas reinhardi was studied with the light and electron microscopes to determine the behavior of flagella in the living cell and the structure of the basal apparatus of the flagella. During normal forward swimming the flagella beat synchronously in the same plane, as in the human swimmer's breast stroke. The form of beat is like that of cilia. Occasionally cells swim backward with the flagella undulating and trailing the cell. Thus the same flagellar apparatus produces two types of motion. The central pair of fibers of both flagella appear to lie in the same plane, which coincides with the plane of beat. The two basal bodies lie in a V configuration and are joined at the top by a striated fiber and at the bottom by two smaller fibers. From the area between the basal bodies four bands of microtubules, each containing four tubules, radiate in an X-shaped pattern, diverge, and pass under the cell membrane. Details of the complex arrangement of tubules near the basal bodies are described. It seems probable that the connecting fibers and the microtubules play structural roles and thereby maintain the alignment of the flagellar apparatus. The relation of striated fibers and microtubules to cilia and flagella is reviewed, particularly in phytoflagellates and protozoa. Structures observed in the transitional region between the basal body and flagellar shaft are described and their occurrence is reviewed. Details of structure of the flagellar shaft and flagellar tip are described, and the latter is reviewed in detail.


1988 ◽  
Vol 107 (2) ◽  
pp. 635-641 ◽  
Author(s):  
J L Salisbury ◽  
A T Baron ◽  
M A Sanders

Monoclonal and polyclonal antibodies raised against algal centrin, a protein of algal striated flagellar roots, were used to characterize the occurrence and distribution of this protein in interphase and mitotic Chlamydomonas cells. Chlamydomonas centrin, as identified by Western immunoblot procedures, is a low molecular (20,000-Mr) acidic protein. Immunofluorescence and immunogold labeling demonstrates that centrin is a component of the distal fiber. In addition, centrin-based flagellar roots link the flagellar apparatus to the nucleus. Two major descending fibers extend from the basal bodies toward the nucleus; each descending fiber branches several times giving rise to 8-16 fimbria which surround and embrace the nucleus. Immunogold labeling indicates that these fimbria are juxtaposed to the outer nuclear envelope. Earlier studies have demonstrated that the centrin-based linkage between the flagellar apparatus and the nucleus is contractile, both in vitro and in living Chlamydomonas cells (Wright, R. L., J. Salisbury, and J. Jarvik. 1985. J. Cell Biol. 101:1903-1912; Salisbury, J. L., M. A. Sanders, and L. Harpst. 1987. J. Cell Biol. 105:1799-1805). Immunofluorescence studies show dramatic changes in distribution of the centrin-based system during mitosis that include a transient contraction at preprophase; division, separation, and re-extension during prophase; and a second transient contraction at the metaphase/anaphase boundary. These observations suggest a fundamental role for centrin in motile events during mitosis.


1976 ◽  
Vol 69 (1) ◽  
pp. 106-125 ◽  
Author(s):  
D L Brown ◽  
A Massalski ◽  
R Patenaude

The organization of microtubular systems in the quadriflagellate unicell Polytomella agilis has been reconstructed by electron microscopy of serial sections, and the overall arrangement confirmed by immunofluorescent staining using antiserum directed against chick brain tubulin. The basal bodies of the four flagella are shown to be linked in two pairs of short fibers. Light microscopy of swimming cells indicates that the flagella beat in two synchronous pairs, with each pair exhibiting a breast-stroke-like motion. Two structurally distinct flagellar rootlets, one consisting of four microtubules in a 3 over 1 pattern and the other of a striated fiber over two microtubules, terminate between adjacent basal bodies. These rootlets diverge from the basal body region and extend toward the cell posterior, passing just beneath the plasma membrane. Near the anterior part of the cell, all eight rootlets serve as attachment sites for large numbers of cytoplasmic microtubules which occur in a single row around the circumference of the cell and closely parallel the cell shape. It is suggested that the flagellar rootless may function in controlling the patterning and the direction of cytoplasmic microtubule assembly. The occurrence of similar rootlet structures in other flagellates is briefly reviewed.


2021 ◽  
Vol 18 (174) ◽  
pp. 20200660
Author(s):  
Hanliang Guo ◽  
Yi Man ◽  
Kirsty Y. Wan ◽  
Eva Kanso

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.


1986 ◽  
Vol 83 (1) ◽  
pp. 135-140
Author(s):  
I.B. Heath ◽  
S.G. Kaminskyj ◽  
T. Bauchop

The controversial question of the possible autonomy of centrioles, as shown by the persistence of all or part of them in the generative cell line throughout the life cycle of organisms, remains unresolved. All previous reports on shedding or withdrawal of cilia and flagella showed that their basal bodies (= centrioles) were retained in the cells where they may, or may not, subsequently disassemble. We show that in the fungus Neocallimastix sp. the basal bodies are discarded with the flagella when zoospores encyst. This shedding of basal bodies argues against centriolar persistence in any form and thus against their autonomy and endosymbiotic origin.


2009 ◽  
Vol 20 (6) ◽  
pp. 1865-1877 ◽  
Author(s):  
Brady P. Culver ◽  
Janet B. Meehl ◽  
Thomas H. Giddings ◽  
Mark Winey

Cilia and flagella are structurally and functionally conserved organelles present in basal as well as higher eukaryotes. The assembly of cilia requires a microtubule based scaffold called a basal body. The ninefold symmetry characteristic of basal bodies and the structurally similar centriole is organized around a hub and spoke structure termed the cartwheel. To date, SAS-6 is one of the two clearly conserved components of the cartwheel. In some organisms, overexpression of SAS-6 causes the formation of supernumerary centrioles. We questioned whether the centriole assembly initiation capacity of SAS-6 is separate from or directly related to its structural role at the cartwheel. To address this question we used Tetrahymena thermophila, which expresses two SAS-6 homologues, TtSAS6a and TtSAS6b. Cells lacking either TtSAS6a or TtSAS6b are defective in new basal body assembly. TtSas6a localizes to all basal bodies equally, whereas TtSas6b is enriched at unciliated and assembling basal bodies. Interestingly, overexpression of TtSAS6b but not TtSAS6a, led to the assembly of clusters of new basal bodies in abnormal locations. Our data suggest a model where TtSAS6a and TtSAS6b have diverged such that TtSAS6a acts as a structural component of basal bodies, whereas TtSAS6b influences the location of new basal body assembly.


2009 ◽  
Vol 106 (37) ◽  
pp. 15567-15572 ◽  
Author(s):  
Aparna Baskaran ◽  
M. Cristina Marchetti

Unicellular living organisms, such as bacteria and algae, propel themselves through a medium via cyclic strokes involving the motion of cilia and flagella. Dense populations of such “active particles” or “swimmers” exhibit a rich collective behavior at large scales. Starting with a minimal physical model of a stroke-averaged swimmer in a fluid, we derive a continuum description of a suspension of active organisms that incorporates fluid-mediated, long-range hydrodynamic interactions among the swimmers. Our work demonstrates that hydrodynamic interactions provide a simple, generic origin for several nonequilibrium phenomena predicted or observed in the literature. The continuum model derived here does not depend on the microscopic physical model of the individual swimmer. The details of the large-scale physics do, however, differ for “shakers” (particles that are active but not self-propelled, such as melanocytes) and “movers” (self-propelled particles), “pushers” (most bacteria) and “pullers” (algae like Chlamydomonas). Our work provides a classification of the large-scale behavior of all these systems.


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