Microtubules and the propagation of bending waves by the archigregarine, Selenidium fallax

1980 ◽  
Vol 87 (1) ◽  
pp. 149-161
Author(s):  
J. S. Mellor ◽  
H. Stebbings

1. The trophozoites of Selenidium fallax propagate bending waves at rates of up to 35 microns s-1, of a similar character to those manifested by eukaryotic cilia and flagella. A beat frequency of 0.12-0.15 Hz appears average, though rates outside this range have been recorded. Translatory locomotion at up to 6 microns s-1 has been observed. The protozoan demonstrates the presence of an active bending mechanism, probably along its entire length, and a means of coordinating adjacent bends. 2. The Reynolds number for the motion in 10(−5)-10(−4), suggesting that the hydrodynamic aspects of the trophozoite movement are amenable to analysis by similar means to those already employed for cilia and flagella. 3. It is possible that the protozoans exhibit a sliding microtubule mechanism, which could be very usefully compared with that occurring in the ciliary axoneme.

2010 ◽  
Vol 189 (3) ◽  
pp. 601-612 ◽  
Author(s):  
Christen G. DiPetrillo ◽  
Elizabeth F. Smith

For all motile eukaryotic cilia and flagella, beating is regulated by changes in intraciliary calcium concentration. Although the mechanism for calcium regulation is not understood, numerous studies have shown that calmodulin (CaM) is a key axonemal calcium sensor. Using anti-CaM antibodies and Chlamydomonas reinhardtii axonemal extracts, we precipitated a complex that includes four polypeptides and that specifically interacts with CaM in high [Ca2+]. One of the complex members, FAP221, is an orthologue of mammalian Pcdp1 (primary ciliary dyskinesia protein 1). Both FAP221 and mammalian Pcdp1 specifically bind CaM in high [Ca2+]. Reduced expression of Pcdp1 complex members in C. reinhardtii results in failure of the C1d central pair projection to assemble and significant impairment of motility including uncoordinated bends, severely reduced beat frequency, and altered waveforms. These combined results reveal that the central pair Pcdp1 (FAP221) complex is essential for control of ciliary motility.


2021 ◽  
Author(s):  
Azam Gholami ◽  
Raheel Ahmad ◽  
Albert J Bae ◽  
Alain Pumir ◽  
Eberhard Bodenschatz

The beating of cilia and flagella is essential to perform many important biological functions, including generating fluid flows on the cell surface or propulsion of micro-organisms. In this work, we analyze the motion of isolated and demembranated flagella from green algae Chlamydomonas reinhardtii, which act as ATP-driven micro-swimmers. The waveform of the Chlamydomonas beating flagella has an asymmetric waveform that is known to involve the superposition of a static component, corresponding to a fixed, intrinsic curvature, and a dynamic wave component traveling in the base-to-tip direction at the fundamental beat frequency, plus higher harmonics. Here, we demonstrate that these modes are not sufficient to reproduce the observed flagella waveforms. We find that two extra modes play an essential role to describe the motion: first, a time-symmetric mode, which corresponds to a global oscillation of the axonemal curvature, and second, a secondary tip-to-base wave component at the fundamental frequency that propagates opposite to the dominant base-to-tip wave, albeit with a smaller amplitude. Although the time-symmetric mode cannot, by itself, contribute to propulsion (scallop theorem), it does enhance the translational and rotational velocities of the flagellum by approximately a factor of 2. This mode highlights a long-range coupled on/off activity of force-generating dynein motors and can provide further insight into the underling biology of the ciliary beat.


1978 ◽  
Vol 76 (1) ◽  
pp. 85-104 ◽  
Author(s):  
YUKIO HIRAMOTO ◽  
SHOJI A. BABA

Computerized analyses were performed on the movement of spermatozoa recorded with a high-speed camera. These provide evidence for active bending waves over the entire length of the flagellum and a single equation for waves in all cases examined. In the equation, the angular direction of the flagellum at any distance from the base is expressed by a sine function of time plus a constant, and thus flagellar waves are ‘sine-generated’. To explain the waves a model was proposed in which the active force required to generate sliding between peripheral microtubules is propagated along and around the flagellar axoneme.


1973 ◽  
Vol 13 (2) ◽  
pp. 337-357 ◽  
Author(s):  
BARBARA H. GIBBONS ◽  
I. R. GIBBONS

Sea-urchin sperm were extracted with o.5 M KCl for 45 s at room temperature in the presence of Triton X-100, and then transferred to reactivating solution containing 1 mM ATP. The flagellar beat frequency of these KCl-extracted sperm (16 beats/s) was only about half that of control Triton-extracted sperm that had not been exposed to 0.5 M KCl (31 beats/s), although the form of their bending waves was not significantly altered. Examination by electron microscopy showed that the extraction with 0.5 M KCl removed the majority of the outer arms from the doublet tubules, leaving the inner arms apparently intact. By varying the duration of the KCl-extraction, it was shown that the rate of decrease in beat frequency paralleled the rate of disappearance of the arms. Prolonging the extraction time beyond 45 s at room temperature, or 4 min at o °C, had little further effect on beat frequency. ATPase measurements suggested that 6o-65% of the dynein in the original axonemes had been solubilized when the extraction with KCl was permitted to go to completion. These results indicate that the generation and propagation of flagellar bending waves of essentially typical form are not prevented by the removal of the outer row of dynein arms from the doublet tubules. In terms of the sliding filament model of flagellar bending, the results suggest that the rate of sliding between tubules under these conditions is proportional to the number of dynein arms present. The lack of significant change in wave form implies that the total amount of sliding that occurs during each bending cycle is not affected by the reduced number of dynein arms, but is regulated independently in some manner by the elastic forces generated by other structures in the bent axoneme.


2005 ◽  
Vol 16 (10) ◽  
pp. 5004-5012 ◽  
Author(s):  
Noveera T. Ahmed ◽  
David R. Mitchell

Dynein motors of cilia and flagella function in the context of the axoneme, a very large network of microtubules and associated proteins. To understand how dyneins assemble and attach to this network, we characterized two Chlamydomonas outer arm dynein assembly (oda) mutants at a new locus, ODA16. Both oda16 mutants display a reduced beat frequency and altered swimming behavior, similar to previously characterized oda mutants, but only a partial loss of axonemal dyneins as shown by both electron microscopy and immunoblots. Motility studies suggest that the remaining outer arm dyneins on oda16 axonemes are functional. The ODA16 locus encodes a 49-kDa WD-repeat domain protein. Homologues were found in mammalian and fly databases, but not in yeast or nematode databases, implying that this protein is only needed in organisms with motile cilia or flagella. The Chlamydomonas ODA16 protein shares 62% identity with its human homologue. Western blot analysis localizes more than 90% of ODA16p to the flagellar matrix. Because wild-type axonemes retain little ODA16p but can be reactivated to a normal beat in vitro, we hypothesize that ODA16p is not an essential dynein subunit, but a protein necessary for dynein transport into the flagellar compartment or assembly onto the axoneme.


1979 ◽  
Vol 82 (2) ◽  
pp. 401-411 ◽  
Author(s):  
C J Brokaw

Asymmetrical bending waves can be obtained by reactivating demembranated sea urchin spermatozoa at high Ca2+ concentrations. Moving-film flash photography shows that asymmetrical flagellar bending waves are associated with premature termination of the growth of the bends in one direction (the reverse bends) while the bends in the opposite direction (the principal bends) grow for one full beat cycle, and with unequal rates of growth of principal and reverse bends. The relative proportions of these two components of asymmetry are highly variable. The increased angle in the principal bend is compensated by a decreased angle in the reverse bend, so that there is no change in mean bend angle; the wavelength and beat frequency are also independent of the degree of asymmetry. This new information is still insufficient to identify a particular mechanism for Ca2+-induced asymmetry. When a developing bend stops growing before initiation of growth of a new bend in the same direction, a modification of the sliding between tubules in the distal portion of the flagellum is required. This modification can be described as a superposition of synchronous sliding on the metachronous sliding associated with propagating bending waves. Synchronous sliding is particularly evident in highly asymmetrical flagella, but is probably not the cause of asymmetry. The control of metachronous sliding appears to be unaffected by the superposition of synchronous sliding.


2017 ◽  
Vol 14 (130) ◽  
pp. 20170065 ◽  
Author(s):  
Rachel Coy ◽  
Hermes Gadêlha

Cross-linked filament bundles, such as in cilia and flagella, are ubiquitous in biology. They are considered in textbooks as simple filaments with larger stiffness. Recent observations of flagellar counterbend, however, show that induction of curvature in one section of a passive flagellum instigates a compensatory counter-curvature elsewhere, exposing the intricate role of the diminutive cross-linking proteins at large scales. We show that this effect, a material property of the cross-linking mechanics, modifies the bundle dynamics and induces a bimodal L 2 − L 3 length-dependent material response that departs from the Euler–Bernoulli theory. Hence, the use of simpler theories to analyse experiments can result in paradoxical interpretations. Remarkably, the counterbend dynamics instigates counter-waves in opposition to driven oscillations in distant parts of the bundle, with potential impact on the regulation of flagellar bending waves. These results have a range of physical and biological applications, including the empirical disentanglement of material quantities via counterbend dynamics.


1976 ◽  
Vol 71 (3) ◽  
pp. 823-831 ◽  
Author(s):  
B H Gibbons ◽  
K Ogawa ◽  
I R Gibbons

Rabbit antiserum prepared against an ATPase-containing tryptic fragment of dynein by Ogawa and Mohri (J. Biol. Chem. 250: 6476-6483) specifically inhibited the ATPase activity of dynein 1 and not that of dynein 2. Varying amounts of this antidynein 1 serum were added to demembranated sperm while they were swimming in reactivating solution containing 1 mM ATP. The sperm continued to form regularly propagated flagellar bending waves, but the beat frequency decreased gradually with time, the greater part of the change occurring in the first 15 min. The beat frequency after 1 h was a function of the amount of antiserum used, and could be as low as 1 Hz. The waveforms of the treated sperm resembled those of normal reactivated sperm except that the bend angles of both the principal and reverse bends were larger in the proximal portion of flagellum. The ATPase activity and corresponding beat frequency of sperm which had been pretreated with varying amounts of antidynein 1 serum for 15 min at 0 degrees C and then diluted were both decreased as a function of the amount of antiserum added, the ATPase activity of homogenized, nonmotile sperm also decreased upon pretreatment with antiserum, but the percentage decrease was less than for motile sperm. For moderate to low concentrations of antiserum, the rates of reaction with motile and with rigor sperm were almost identical. The overall results suggest that antidynein 1 inhibits the functioning of the dynein arms, probably by blocking the ATPase sites of the dynein 1.


2022 ◽  
Author(s):  
Veikko F. Geyer ◽  
Jonathon Howard ◽  
Pablo Sartori

AbstractBiological systems are robust to perturbations at both the genetic and environmental levels, although these same perturbations can elicit variation in behaviour. The interplay between functional robustness and behavioural variability is exemplified at the organellar level by the beating of cilia and flagella. Cilia are motile despite wide genetic diversity between and within species, differences in intracellular concentrations of ATP and calcium, and considerable environment fluctuations in temperature and viscosity. At the same time, these perturbations result in a variety of spatio-temporal patterns that span a rich behavioural space. To investigate this behavioural space we analysed the dynamics of isolated cilia from the unicellular algae Chlamydomonas reinhardtii under many different environmental and genetic conditions. We found that, despite large changes in beat frequency and amplitude, the space of waveform shapes is low-dimensional in the sense that two features account for 80% of the observed variation. The geometry of this behavioural space accords with the predictions of a simple mechanochemical model in the low-viscosity regime. This allowed us to associate waveform shape variability with changes in only the curvature response coefficients of the dynein motors.


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