1. The translational and turning movements of the spore of Blastocladiella emersonii are described.

  2. The turning movement appears to be a direct result of asymmetric flagellar activity.

  3. The results indicate that co-ordination of propagated waves may not be exclusively effected by a system which involves the mechanical properties of the flagellum but also by stimuli derived from another source.

Although the random nature of the movement of some plant spermatozoa has been described (Wilkie, 1954; Brokaw, 1959) and the influences of concentration and voltage gradients on the movement have been discussed (Pfeffer, 1884; Brokaw, 1957, 1958 a, b, 1959), no account of the flagellar movement of this type of organism has been given.

Two possible mechanisms which could be responsible for the turning of flagellated organisms in response to the presence of chemotactically active ions have been suggested. Re-orientation of an organism could be brought about by variation in the activity of the flagella (Hoyt, 1910; Metzner, 1926; Brokaw, 1958b) or by the action of an electric field on ions absorbed on a region of the cell (Brokaw, 1958a).

This paper records the results of a high-speed cine-photographic study of the movement of the spore of Blastocladiella emersonii with special reference to the turning movement. The results are discussed in the light of current hypotheses of flagellar wave propagation.

During forward movement of the organism almost planar waves of lateral displacement pass from base to tip along the flagellum as shown in Pl. 1. Certain parts of the flagellum appear more sharply focused than others, suggesting that there is a threedimensional component to the wave movement. Average values for the various wave parameters and translational velocity of the organism are summarized in Table 1.

Table 1.

The wave parameters of B. emersonii spores

The wave parameters of B. emersonii spores
The wave parameters of B. emersonii spores

A striking feature of the behaviour of this organism is the abrupt way in which the direction of motion may change. Plate 2 shows a spore executing a turn. Immediately prior to fig. 2 (Pl. 2) the spore was moving normally with waves passing from base to tip. The waveform in fig. 2 (Pl. 2) has the appearance of a normal progressive wave but only the more distal wave progresses to the tip of the flagellum; the bend at the proximal end of the flagellum does not progress in the usual way, so that at this stage (Pl. 2, fig. 4) the greater part of the flagellum is quiescent. In the period between figs. 4 and 7 (Pl. 2) no progressive waves are present on the flagellum and the distal region executes a motion which resembles spatially half a cycle of a standing wave in that there are nodes a few microns from either end of the flagellum. A set of superimposed tracings from regularly spaced (temporally) frames of a cine film illustrating the presence of the nodes is shown in Text-fig. 1. During this same period (i.e. Pl. 2, figs. 4-7) the head of the spore turns towards the flagellum through a large angle in the plane of the original flagellar beating as though pivoted at a point on its longitudinal axis a few microns from the base of the flagellum. Normal wave movement begins again at Pl. 2, fig. 8, with the result that the head turns in the reverse direction. By the time a complete wave is established on the flagellum and normal forward motion begins again, the head has turned back through an angle equal to about half the maximum angular displacement (see Text-fig. 2). Text-fig. 2 records the orientation of the head as a function of time with respect to an arbitrary axis stationary relative to the laboratory. The undulations shown in this figure at times before and after the turn record the normal oscillatory movement of the head during progressive motion in one direction.

Text-fig. 1.

Superimposed tracings made from a sequence of frames from a high-speed cine film of the turning movement of the spore of B. emersonii. Notice the standing wave pattern on the distal region of the flagellum.

Text-fig. 1.

Superimposed tracings made from a sequence of frames from a high-speed cine film of the turning movement of the spore of B. emersonii. Notice the standing wave pattern on the distal region of the flagellum.

Text-fig. 2.

Variation of angle (measured with respect to an arbitrary datum line) with time during a single turn of the spore of B. emertonii.

Text-fig. 2.

Variation of angle (measured with respect to an arbitrary datum line) with time during a single turn of the spore of B. emertonii.

Flagella of spores which are attached to the slide support distally propagating waves with frequent interruptions to follow a manoeuvre corresponding to the turning motion. In this condition the head may remain motionless while the flagellum executes its movements.

The flagellar motion which is observed during the turning movement of B. emersonii spores may be the cause or the effect of the change in orientation of the organism. That it is probably the cause is indicated by the observation of flagella of organisms which are non-motile by virtue of being attached to the slide. If the turning movement were responsible for the asymmetry in the flagellar movement then, when the organism is prevented from turning, the flagellum should undulate rhythmically with no interruptions, a situation which is not observed in practice.

It therefore seems possible that in organisms which turn in response to a gradient of voltage or of concentration of chemotactically active ion the flagellar activity is controlled in a manner dictated by the external influence. This appears to be true in the case of Allomyces, which has a single flagellum and turns in response to a concentration gradient of syrenin in the same way as the spores of B. emersonii (M. J. Carlile, C. A. Miles & M. E. J. Holwill, in preparation). A similar mechanism may also be operative in chemotactic turning of the monoflagellate gamete of Campamdaria (Miller, 1966; R. L. Miller & C. J. Brokaw, personal communication), and in the turning (probably not chemotactic) of sea-urchin spermatozoa (C. J. Brokaw & M. E. J. Holwill, unpublished results). When the organism has several flagella, as in the bracken spermatozoid, the mechanisms may be different, and a complete evaluation of the system in this case must await further investigation.

Such an organism might turn as the result of asymmetric bending of some or all its flagella; alternatively, the flagella on one side of the organism may stop beating completely for the duration of a turn, thus allowing the undulating flagella on the other side to provide an asymmetric thrust on the organism as a whole. In his earlier work on the chemotaxis of fern spermatozoids Brokaw (1958a) cites the constancy of translational speed during a turn as a reason for supposing that flagella are not directly responsible for chemotactic orientation. If, however, only some of the many flagella on this organism are responsible for the turning movement while the remainder beat with their normal frequency, wavelength and amplitude, little variation in swimming speed would be observed (Holwill & Burge, 1963).*

In a later publication Brokaw (1958 b) reports new results which conflict with his original suggestions and lead him to reject, for bracken spermatozoids at least, a mechanism for chemotactic turning involving chemophoresis in favour of a system which can modify the flagellar movement when influenced by the presence of chemotactively active ions.

If asymmetry in the flagellar beating is responsible for the turning movement of B. emersonii spores, then some conclusions about the properties of the mechanism underlying wave propagation may be drawn. Two hypotheses for wave propagation, both of which utilize the elastic properties of the flagellum, have been proposed (Machin, 1958, 1963; Brokaw, 1966). Both theories suppose that units for actively bending the flagellum are located throughout the length of a flagellum and that a unit can be activated on being deformed by passive bending. (The term ‘unit’ is used here merely for convenience and is not to be interpreted as placing a restriction on the type of mechanism which might bend the flagellum. For example, the unit may be capable of active contraction or it could be part of a sliding filament system.)

According to Machin (1958, 1963) the units serve to amplify the passive wave propagated along the flagellum. Brokaw’s (1966) theory is based on observations which indicate that flagellar waves consist of circular arcs linked by straight lines (Brokaw & Wright, 1963; Brokaw, 1965). Transition of an element from the straight to the curved state is supposed to be abrupt, and passive bending is assumed to spread locally ahead of a transition region. Both hypotheses require a bend to pass along the flagellum, once it is established, with a velocity determined essentially by the elastic constants of the flagellum and the viscosity of the medium. On Machin’s theory all the units are autonomous oscillators, whereas Brokaw supposes that autonomous oscillation is confined to a pacemaker in the basal region of the flagellum.

The flagellar motion which occurs during the turning of B. emersonii spores suggests that considerable control can be exerted over the movement of the flagellum. If wave propagation is entirely mechanical, then control of flagellar movements could be effected by modifying the physical boundary conditions that exist at either end of the flagellum.

Alternatively, direct control of wave motion could be imposed on the flagellum at regions remote from its base. In this case, stimuli that are independent of the elastic properties of the flagellum might be used, either by themselves or as a supplement to mechanical or other wave propagation, to co-ordinate the wave motion.

Further experiments are in progress to investigate the properties of the control system.

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Plate 1

Plate 1

The spore of B. emersonii. A sequence of frames showing flagellar activity during translational movement. Total elapsed time = 20 msec.

Plate 1

The spore of B. emersonii. A sequence of frames showing flagellar activity during translational movement. Total elapsed time = 20 msec.

Plate 2

Plate 2

The turning movement of the spore of B. emersonii. For explanation see text. Total elapsed time = 125 msec.

Plate 2

The turning movement of the spore of B. emersonii. For explanation see text. Total elapsed time = 125 msec.

*

Holwill & Burge (1963) have shown that the velocity of an organism propelled by several flagella executing helical undulations becomes essentially constant when the number of flagella present exceeds ten. A similar conclusion is valid for organisms propelled by flagella executing planar waves.