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Phototransduction in Blepharisma and Stentor NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY VOLUME 34 NUMBER 1 http://rcin.org.pl WARSAW, POLAND 1995 ISSN 0065-1583 Polish Academy of Sciences Nencki Institute of Experimental Biology ACTA PROTOZOOLOGICA Internationa! Journal on Protistology Editor in Chief Jerzy SIKORA Editors Hanna FAB CZAK and Anna WASIK Managing Editor Małgorzata WORONOWICZ Editorial Board Andre ADOUTTE, Paris Stanisław L. KAZUBSKI, Warszawa Christian F. BARDELE, Tübingen Leszek KUZNICKI, Warszawa, Chairman Magdolna Cs. BERECZKY, Göd John J. LEE, New York Jacques BERGER, Toronto Jiri LOM, Ceske Budejovice Y.-Z. CHEN, Beijing Pierangelo LUPORINI, Camerino Jean COHEN, Gif-Sur-Yvette Hans MACHEMER, Bochum John O. CORLISS, Albuquerque Jean-Pierre MIGNOT, Aubiere Gyorgy CSABA, Budapest Yutaka NAITOH, Tsukuba Isabelle DESPORTES-LIVAGE, Paris Jytte R. NILS SON, Copenhagen Stanisław DRYL, Warszawa Eduardo ORIAS, Santa Barbara Tom FENCHEL, Helsingór Dimitrii V. OSSIPOV, St. Petersburg Wilhelm FOISSNER, Salsburg Igor B. RAIKOV, St. Petersburg Vassil GOLEMANSKY, Sofia Leif RASMUSSEN, Odense Andrzej GRĘBECKI, Warszawa, Vice-Chairman Michael SLEIGH, Southampton Lucyna GRĘBECKA, Warszawa Ksenia M. SUKHANOVA, St. Petersburg Donat-Peter HÄDER, Erlangen Jiri VAVRA, Praha Janina KACZANOWSKA, Warszawa Patricia L. WALNE, Knoxville Witold KASPRZAK, Poznań ACTA PROTOZOOLOGICA appears quarterly. © NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY, POLISH ACADEMY OF SCIENCES Printed at the MARBIS, 60 Kombatantów Str., 05-070 Sulejówek, Poland Front cover: Wallackia schiffmanni. In : W. Foissner (1976) Wallackia schiffmanni nov. gen., nov. spec. (Cilio- phora, Hypotrichida) ein alpiner hypotricher Ciliat. Acta Protozool. 15: 387-392 http://rcin.org.pl ACTA Acta Protozoologica (1995) 34: 1 - 11 Review article PROTOZOOLOGICA Phototransduction in Blepharisma and Stentor Stanisław FABCZAK and Hanna FABCZAK Department of Cell Biology, Nencki Institute of Experimental Biology, Warszawa, Poland Summary. The ciliates Blepharisma and Stentor exhibit distinct light-avoiding behavior (photophobic response). This cell behavior is attributed to photoexcitation of receptor chromoproteins located in cell organelles (pigment granules). The photochemical process in the receptors of both these ciliates, considered as a primary reaction to light, initiates the sensory transduction chain leading to delayed generation of membrane photoreceptor potential. The photoreceptor potential is coupled to the photophobic response (ciliary reversal) through an action potential which is elicited by receptor potential when its amplitude exceeds the membrane excitation threshold. The direct relationship between photoelectrical transduction and electromotor events is evidenced by a close temporal correlation observed in Blepharisma and Stentor between the latency periods of the action potential and of the cell stop response (receptor/action potentials appear to be instrumental in initiation of ciliary reversal). The photoreceptor potentials in Blepharisma are generated by transient changes in membrane conductance for Ca2+ ions. In Stentor the ionic nature of light-dependent membrane depolarization has not been fully elucidated. The action potentials in both Blepharisma and Stentor ciliates are produced by any suprathreshold depolarization, such as a photoreceptor potential, in the consequence of the Ca2+ channel and, after a delay, the K+ channel activations. Key words. Photoreceptor potential, action potential, photophobic response, Blepharisma, Stentor, sensory transduction. INTRODUCTION membrane-vesicle granules of about 0.3-0.7 |j.m in diameter. The pigment granules are located in the vicinity The pink Blepharisma japonicum and related blue- of ciliary basal bodies, directly under the cell pellicle. They green Stentor coeruleus ciliates are known to respond to are distributed in regular pigmented rows, alternating with changes in environmental illumination. In an unevenly clear rows of kineties over the cell body surface (Huang illuminated container these cells swim predominantly and Pitelka 1957, Randall and Jackson 1958, Tartar 1961, towards shady or darker areas, away from the light source Kennedy 1965, Giese 1973, Newman 1974). Spec- (photodispersal) (Jennings 1906, Mast 1906, Giese 1973, trophotometric analysis of the pigment structure of Stentor Diehn et al. 1977). Both these protozoa display distinct cells showed that the pigment identified as stentorin sensitivity to light since, unlike most other ciliates, they belongs to meso-naphthodianthrone class of compounds possess specific pigments (photoreceptors) enclosed in (Lankester 1973, Moller 1962, Walker et al. 1979, Tao et al. 1994). The structure of the pigment in Blepharisma, Address for correspondence: S. Fabczak, Department of Cell called blepharismin, has not been fully elucidated yet. Biology, Nencki Institute of Experimental Biology, ul. Pasteura 3, According to Sevenants (1965) blepharismin presumably PL-02-093 Warszawa, Poland; Fax: (4822) 225342; E-mail: [email protected] is also a derivative of hypericin. http://rcin.org.pl 2 S. Fabczak and H. Fabczak Recent experiments on aqueous preparations of pig- of cessation of forward swimming of the cell (stop ment granules from Blepharisma and Stentor provide response) followed by a period of backward swimming some data indicating that the absorption of light energy (ciliary reversal) (Fig. 1). Stentor moves backwards in by cellular pigments is accompanied by a release of H+ a more or less straight line (Figs. 1 b,c) while Blepharis- ions and acidification of the solution (Walker et al. 1981, ma mostly moves backwards along a semicircular path- Matsuoka et al. 1992). The changes in the cytoplasm pH way (Figs. le,f)- After a period of ciliary reversal the of intact Stentor cells under steady-state photic stimula- cell stops its movement before resuming a forward tion have also been shown to occur (Song 1981, Song movement. Between the onset of the applied light et al. 1981). Based on these data, it has been proposed stimulus and the beginning of the cell stop response that the observed rapid proton release from the pigment there is a lag-time the length of which is inversely into cell cytoplasm is an initial signal triggering the proportional to the light intensity (Kraml and Marwan photosensory transduction chain which results in 1983; Scevoli et al. 1987; Iwatsuki and Kobayashi photodispersal of Blepharisma and Stentor cells (Song 1991; Fabczak S. et al. 1993a, b). The delay of response 1981, 1983; Passarelli et al. 1984; Ghetti 1991). in Stentor cells is of 0.1-0.2 s (Wood 1976, Iwatsuki and Kobayashi 1991, Fabczak S. et al. 1993a), and in Blepharisma this delay is longer and is about 1 s (Kraml and Marwan 1983, Ghetti 1991, Fabczak S. et LIGHT-DEPENDENT MOTILE RESPONSES al. 1993b). The overall result of the photophobic response in Blepharisma and Stentor is the change of Photophobic response the forward movement direction and escape from the The photodispersal in Blepharisma and Stentor lighted area. ciliates is a behavioral consequence of different specific The sensitivity of the surface of the cell body to light light-avoiding responses such as negative phototaxis, in Blepharisma as well as in Stentor is not uniform. On positive photokinesis and step-up photophobic respon- light stimulation of different regions of Blepharisma ses. The negative phototaxis is displayed by Stentor body the photophobic response could be more readily when a light beam is applied from a particular direction. elicited by illuminating the anterior part of the cell. On such illumination, the cells tend to turn and swim Illumination of the posterior part of the cell did not evoke away from the light source in a direction parallel to the the photophobic response. In contrast, the acceleration direction of light propagation, both in region where the of swimming (photokinetic response) was elicited to the beam is converging and were it is diverging (Song et al. same extent irrespective which part of the Blepharisma 1980b). The mechanism of cell phototactic response has was subjected to illumination (Kraml and Marwan 1983, not been elucidated in detail but it is supposed to consist Matsuoka 1983b). A similar morphological difference of a series of consecutive and rapid ciliary reversals has been reported in the ciliate Stentor where the anterior (Song 1989). Both in Blepharisma and Stentor there is part of the cell is more sensitive to light stimulation than a distinct dependence of the velocity of their movement the posterior one (Wood and Martinelli 1990). These upon light intensity (photokinesis); the stronger is the differences in responses, similarly as the recent spectro- intensity of illumination of the cells, the greater is the scopic evidence provided for Stentor (Iwatsuki 1991), speed of their swimming (Kraml and Marwan 1983, suggest that the photoreceptors initiating the Matsuoka 1983b, Iwatsuki 1991, Fabczak S. et al. photophobic response are different from those inducing 1993b). Moreover, in Blepharisma, the changes in body the photokinetic effect. length in the order of 50% were reported upon steady- The ciliary reversal which is observed during the state illumination (Matsuoka 1983b, Matsuoka and photophobic response is quite typical and can be evoked Shigenaka 1985). in many ciliates by a variety of stimuli. However, the Most studies on behavioral photoresponses in overall photophobic response in Blepharisma and Sten- Blepharisma and Stentor cells were devoted to the tor differs from their response, for instance,
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