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Bistable Membrane Potential of Coleps Hirtus 759 The Journal of Experimental Biology 203, 757–764 (2000) 757 Printed in Great Britain © The Company of Biologists Limited 2000 JEB2284 BISTABLE MEMBRANE POTENTIAL OF THE CILIATE COLEPS HIRTUS PIA RUDBERG AND OLAV SAND* Department of Biology, University of Oslo, PO Box 1051 Blindern, N-0316 Oslo, Norway *Author for correspondence (e-mail: [email protected]) Accepted 24 November 1999; published on WWW 26 January 2000 Summary In normal recording solution, the swimming pattern of prolonged the shoulder, which occasionally stabilised at the the freshwater ciliate Coleps hirtus, belonging to the class shallow membrane potential (−30 mV). The membrane Prostomatea, consists of alternating periods of nearly linear potential could be shifted to the deep level by brief forward swimming and circular swimming within a small hyperpolarising current injections. Similar biphasic area. Current-clamp recordings were performed to membrane properties have not been reported previously in elucidate the mechanism for this behaviour. No members any ciliate. The bistability of the membrane potential was of this class have previously been studied using abolished in Ca2+-free solution containing Co2+ or Mg2+. In electrophysiological techniques. The ciliates were Ca2+-free solution containing 1 mmol l−1 Ba2+, brief maintained in culture and fed on the planctonic alga depolarising current injections at the deep potential level Rhodomonas minuta. The membrane potential showed evoked all-or-nothing action potentials with a prolonged spontaneous shifts between a more negative (deep) level of plateau coinciding with the shallow potential. We conclude approximately −50 mV and a less negative (shallow) level that the deep membrane potential in C. hirtus corresponds of approximately −30 mV. The input resistance and to the traditional resting potential, whereas the shallow capacitance at the more negative level were approximately level is a Ca2+-dependent plateau potential. In normal 400 MΩ and 120 pF respectively. C. hirtus displayed a solution, the direction of the ciliary beat was backwards at pronounced inward rectification, which was virtually the deep potential level and forwards at the shallow insensitive to 1 mmol l−1 Cs+ and almost completely blocked membrane potential, probably reflecting the two main by 1 mmol l−1 Ba2+. Depolarising current injections failed phases of the swimming pattern. to evoke graded, regenerative Ca2+ spikes. However, current-induced depolarisations from the more negative Key words: Coleps hirtus, ciliate, electrophysiology, membrane potential level (−50 mV) showed a pronounced shoulder potential, bistability, action potential, Ca2+, inward rectification, during the repolarising phase. Increased current injections swimming. Introduction Within the eight different classes of ciliates, approximately found in Bursaridium, from the class Colpodea, which 8000 species have so far been described (Corliss, 1994). generates spontaneous all-or-nothing action potentials with a However, electrophysiological properties have only been distinct threshold in normal solution (Berg and Sand, 1994). studied in a surprisingly small number of species, mainly Spontaneous action potentials with a plateau phase lasting up within the genera Paramecium (Eckert and Naitoh, 1972), to 3–4 s have also been reported in Stylonychia in solutions Stylonychia (Machemer and Deitmer, 1987), Didinium (Pape containing artificially high concentrations of Ca2+ (Machemer, and Machemer, 1986; Pernberg and Machemer, 1989) and 1970). Euplotes (Lueken et al., 1996). The presence of voltage- The ciliate genus Coleps belongs to the class Prostomatea, sensitive Ca2+ channels is a general feature in these ciliates, and no species within this class has previously been studied and the direction of the ciliary beat is controlled by the using electrophysiological methods. The swimming pattern of cytosolic Ca2+ concentration (Machemer and Sugino, 1989; C. hirtus in normal solution consists of forward swimming Pernberg and Machemer, 1995a,b). The detailed electrical covering relatively large distances interrupted by periods membrane properties, however, show great variation among of circular swimming within a small area. We have made different ciliate classes. In most cases, depolarising current current-clamp recordings from C. hirtus using standard injections evoke regenerative Ca2+ spikes lacking all-or- microelectrodes, and report exceptional electrophysiological nothing characteristics in normal solution, for instance in properties of this ciliate. The membrane potential showed Paramecium (see Machemer, 1988), belonging to the class spontaneous shifts between two semistable levels. The more Oligohymenophorea. A striking exception to this pattern is negative level corresponds to the traditional resting potential, 758 P. RUDBERG AND O. SAND whereas the less negative level is a Ca2+-dependent plateau animals were kept in position using a microsuction pipette with potential. The transition between these membrane potential a tip diameter of 10–15 µm. The suction pipette was connected levels was correlated with the reversal of the direction of the to ambient, subatmospheric or superatmospheric pressure via ciliary beat and may explain the characteristic swimming a solenoid valve (Jonsson and Sand, 1987). A selected animal behaviour of this ciliate. was sucked onto the tip of the pipette by activating the solenoid valve, using a manual trigger. The subatmospheric catching pressure was between −1.0 and −1.5 kPa, whereas the holding Materials and methods pressure during the recordings was reduced to −0.5 kPa. The Animals animals are coated with a gel-like material, which tended to Coleps hirtus Nitzsch is a barrel-shaped freshwater ciliate clog the pipette. Between each catch, the pipette was therefore feeding on dead or living algae, flagellates, rotifers or other cleaned using a short flush of medium through the tip. This was protozoa. The genus is characterised by an elaborate achieved by connecting the pipette to a pressure of endoskeleton consisting of superficial rows of calcium approximately 5 kPa. carbonate plates (Fig. 1). The animals were obtained from a The movements of both freely swimming animals and lake near Oslo and kept in culture. They were fed on the ciliates penetrated by microelectrodes were studied using a − planktonic alga Rhodomonas minuta, as described by video camera recording at 25 frames s 1. The general direction Klaveness (1984). The algae were grown in standard growth of the ciliary beat of penetrated cells was determined in a medium (Guillard and Lorenzen, 1972) at 17 °C with a suspension of carmine particles. A rough estimate of the beat 14 h:10 h light:dark photoperiod. The mean length of the direction was obtained from the movements of the insoluble animals in our cultures was 42 µm and the mean width was dye grains (diameter 0.5–1 µm) surrounding the cell. 29 µm (N=60). The cultures of Coleps hirtus and Rhodomonas Simultaneous recordings of the membrane potential and animal minuta were generously provided by Dr Dag Klaveness. and particle movements were stored on separate channels of the same recorder. Recordings Results are reported as means ± S.D. Prior to the recordings, the animals were transferred from the growth medium to a recording solution containing (in −1 Results mmol l ): CaCl2, 1; NaCl, 1; KCl, 1. The solution was adjusted to pH 7.2 with 1 mmol l−1 Tris/HCl. In some Swimming behaviour experiments, the CaCl2 in this normal recording solution was In normal recording solution, the swimming behaviour of C. replaced with BaCl2, CoCl2 or MgCl2. In one series of hirtus consisted largely of two alternating main patterns: experiments, 1 mmol l−1 CsCl was added to the normal forward swimming and circular movements. The forward solution. During the experiments, the animals were viewed swimming usually displayed a component of lateral through an inverted microscope. oscillations of small amplitude. Swimming speed was The electrical properties of the surface membrane were 0.4–1.0 mm s−1. At irregular intervals, the periods of forward studied using conventional microelectrodes and standard swimming were interrupted by circular movements within a recording equipment. The electrodes were filled with 4 mol l−1 restricted area (Fig. 2). The duration of these two swimming potassium acetate adjusted to pH 7.2 with acetic acid, and the patterns varied from a few seconds to more than a minute. electrode resistance was 40–80 MΩ. During the recordings, the The main purpose of the present investigation was to elucidate the cellular mechanisms behind this characteristic swimming pattern. In other ciliate species, the direction of the ciliary beat is controlled by the cytosolic Ca2+ concentration and, hence, the membrane potential. The natural approach was therefore to study the electrophysiological properties of C. hirtus. Passive electrical membrane properties and membrane rectification The initial recordings revealed a bimodal distribution of the membrane potential in normal solution. In approximately 70 % of the cells, the membrane potential was between −50 and −60 mV (deep membrane potential), whereas the remaining − 10 µM cells displayed membrane potentials between 20 mV and −30 mV (shallow membrane potential). To study the resistance, Fig. 1. A drawing of the endoskeleton of Coleps hirtus based on capacitance and rectifying properties of the membrane, hyper- scanning electron micrographs from Klaveness (1984) and Foissner and depolarising current pulses of varying
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