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Analysis of the Mechanism of Dinoflagellate Flagella Contraction-Relaxation Cycle

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Analysis of the Mechanism of Dinoflagellate Flagella Contraction-Relaxation Cycle Biol Cell (1992) 76, 33-42 33 © Elsevier, Paris Original article Analysis of the mechanism of dinoflagellate flagella contraction-relaxation cycle Monique Cachon a, Claude Greuet b, Jacky Cosson a, Philippe Huitorel" a Groupe de Motilitd Cellulaire, URA 671 du CNRS, Universit~ Pet M Curie, Observatoire Ocdanologique, 06230 Villefranche-sur-Mer; b Centre de Biologie Marine, Laboratoire de Cytophysiologie des Protistes, Universitd de Nice-Sophia Antipolis, 06108 Nice Cedex, France (Received 11 May 1992; accepted 29 September 1992) Summary - Dinoflagellates possess two flagella. One of them, the longitudinal flagellum, retracts from time to time in some species, such as Ceratium and Peridinium. Additional structures which run along the axoneme seem to be responsible for this particular beha- viour. The retraction which is rapid (less than 60 ms) may be subdivided into several steps: i) the undulating movement stops; ii) the flagellum appears then as a jagged line during 20 ms; iii) finally a rapid retraction (20 ms) takes place, the flagellum being folded 20 times inside the cylindrical flagellar pocket. The measurements on video-records suggest that the R-fibre shortens to 30°7o of its original length. The contraction and relaxation mechanism of nanofilaments is proposed to be through coiling and uncoiling depen- dent on Ca 2+ concentration. protist / flagellar contraction / nanofilaments Introduction Motility observations Dinoflagellates possess two flagella, one longitudinal and These were made using Leitz and Reichert microscopes equipped one transverse, whose properties are not yet fully under- with differential interference contrast (DIC) Nomarski optics. stood [1-10]. These flagella appear to beat according to Video recordings were made with a Panasomic CCD camera sinusoidal waves [11] but in fact the transverse has a heli- (F. 15) combined with a Hamamatsu real time image processor cal beat while the longitudinal has a planar wave. How- (DVS-3000) and a Sony Umatic or a Panasomic Super VHS video tape recorder. Some sequences were obtained with a strobosco- ever, in and the longitudinal Ceratium Peridinium, pic light source operated at 50 Hz. Photographs of still frames flagellum, which is one of the thickest flagella ever obser- on monitor were obtained on Technical Pan 2415 Kodak film ved, shows an original property: it is able to retract and exposed for I/8 s. A NAC high speed video camera was also used relax like a spring [1, 4, 10, 12]. at 200 frames/s. Next to the axoneme, and running parallel to it, are asso- ciated filamentous structures [5, 10] made of contractile but non-actin filaments, the nanofilaments [8, 9] also observed in the cytoplasm of Dinoflagellates [13-16] Electron microscopy which might be responsible for this special behaviour: the retraction of the longitudinal flagellum. Fixation was performed mostly according to Maruyama [5]. The cells were fixed with a 0.1-M phosphate buffered fixative (pH 7.4-7.8) containing 507o glutaraldehyde, 0.8-1 M glucose at room temperature for 1 h. Then they were washed in a buffer contain- ing 0.3 M phosphate and 0.8 M glucose. After treatment by 207o Materials and methods OsO 4 in phosphate-glucose buffer for approximately l h a decreasing graded series of phosphate-glucose solutions were Biological materials used, before a progressive dehydratation. Finally, they were embedded in Spurr's low viscosity medium [17]. The sections were The marine organisms were collected from surface layers with stained wiht 907o uranyl acetate in methanol followed by lead a fine meshed net in the Villefranche-sur-Mer bay during the win- citrate and examined with a Hitachi H603 electron microscope. ter and spring months and from Sugashima Bay (Japan) from Flagella are generally preserved in situ with difficulty, because September to November 1991. Individual cells were isolated with the fixative itself acts as a contracting agent and the calcium as small pipettes (about 50/~m in diameter) and maintained in Petri a triggering retraction agent. To preserve flagella the organisms dishes containing sea water till video-records or electron- were trapped among fibres of nucleohistones [18], this method microscopical fixations were made. allowing also an easier handling of the Protists. Several species of Ceratium have been studied: our observa- Ca2+-free artificial sea water was used to prevent contraction tions were mainly made on Cfurca Ehrenberg, C tripos Mtiller, of flagella (477 mM NaCl, 97 mM KC1, 20.9 mM MgCl 2, C gravidum Gourret and C limulus Gourret. These species are 27.6 mM MgSO4, 5 mM ethyleneglycol his (fl-aminoethylether) almost flat and their two flagella originate from the middle of N,N-tetraacetic acid (EGTA) and 30 mM Tris-HCl (pH 7.6). The the ventral area out of a widely opened cylindrical pocket (fla- living organisms were briefly washed in this medium prior to gellar pocket). fixation. 34 Monique Cachon et al Fig 1. The longitudinal flagellum (fl) is visualized extended (a), straight across the flagellar pocket (fp) the organism, transferred into Ca2+-free sea-water, is observed by DIC optics contrast microscopy (x 1200) or contracted (b) and folded inside the flagellar pocket (living organism; video recording of DIC images, x 1500) scale bar = 10 tzm. Computer image treatments of electron micrographs nal agents [4] such as mechanical shocks, the flagellum retracts suddenly inside the flagellar pocket (figs lb, 2B). The electron micrographs have been digitized with a scanner and It disappears inside the pocket in less than three video processed on a computer to extract 'skeletons' of the structures frames of 1/50 s that is, in less than 60 ms, its distal extre- by further contrast enhancement. mity often remaining outside and uncoiled. We used the GT 4000 Epson Colour Image Scanner connec- Even though the retraction appears to be rapid, we could ted to an IBM PC operated under EpscanIlI. The digitized ima- ges were then treated by varying several parameters, using the visualize different stages of retraction by studying many Paintbrush software. video sequences. It can be subdivided into four steps: 1) the sinusoidal waves stop (fig 3b); 2) a shiver propa- gates from the base of the flagellum towards its distal tip within 20 ms though Maruyama said the retraction was Results in the reverse direction. Bending points appear every 9 ~zm (fig 3b). A jagged line is thus observed located in a plane, Video-microscopical observations each segment of 9 ~m becoming two segments of 4.5 tzm in length (figs 3c, 4a); 3) the next step of the retraction The longitudinal flagellum originates from an unusually takes place in 20 ms (figs 3d, 4b, c). The flagellum shows long (1.5/zm) basal body located at the bottom of a deep 20 folds, the length of each segment remaining constant cylindrical flagellar pocket (about 6/zm in diameter and throughout the contraction process. The distance between 16/~m in length). It can be easily observed (fig la) with a bend of the flagellum and the next one shortens down DIC optics. The two cartoons of figure 2 show the beha- to about 0.6 ~m. The folds are adjacent to each other and viour of the flagellum in the relaxed state (fig 2A) and the in the same place (fig 4b); 4) soon after the complete retrac- contracted state (fig 2B). On one side of the basal body tion the fold topology changes: the 3rd fold slides under (see the diagram; fig 2), the cytostome is located with its the 1st fold, the 4th fold under the 2nd fold... (fig 4c). aperture close to the base of the flagellum. A large pusule Finally the flagellum is inside the pocket, its folds being opens on the other side and contracts periodically to eject tightly squeezed together. The planes in which they are waste products and liquid. located define a right-handed helix as was already sugges- Analysis of video-recordings shows that sinusoidal ted by Maruyama [4]. waves are normally propagated along this flagellum The duration of the contracted state is variable from one (fig 3a), and that they appear as perfect sine waves com- second to several minutes. When the organism is still in sea posed of arcs and straight segments in between curved water, the flagellum contracts very rarely. Conversely, after portions. a long time of observation, when it is exhausted, the flagel- As the cells are heavily armoured (thecate), they do not lum may then contract very frequently without interruption. move rapidly. However, it is easier to study the behaviour In contrast to the contraction, the relaxation is much of their flagella when the cell bodies are stuck on the glass slower (about 1/5 s): the flagellum unfolds slowly from surface because the flagellum remains in focus. The wave its base propagating sinusoidal waves progressively amplitude is limited in the flageliar pocket but its frequency towards its tip, still folded and crumpled, until the very is the same as outside the pocket, the aperture of the pocket end of the relaxation process (fig 5). playing the role of a node of beating. The flagella which have been broken by manipulations Spontaneously, and perhaps under the action of exter- regrow in 2-3 h. Analysis of the mechanism of dinoflagellate flagella contraction-relaxation cycle 35 Fig 2. These two schematic drawings propose an interpretation of the behaviour of the longitudinal flagellum of Ceratium furca. A. The flagellum emerging from its basal body (bb) located between the cytostome (cyt) and the pusule (pu), extends from the flagel- lar pocket (Fp) while it is relaxed. B. While it is contracted, the flagellum is located entirely inside the flagellar pocket which appears then to be almost closed by a thin membranous operculum.
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