Membrane Excitability and Motile Responses in the Protozoa, with Particular Attention to the Heliozoan Actinocoryne contractilis

  • Colette Febvre-Chevalier
  • André Bilbaut
  • Jean Febvre
  • Quentin Bone
Part of the NATO ASI Series book series (NSSA, volume 188)


Unicellular microorganisms are regarded as primitive eukaryotes. However, they are extremely adaptable and display a remarkable diversity of shape, behavior and mode of life. They are sensitive to various stimuli (Naitoh, 1982; Machemer and Deitmer, 1987) and the response to external signals is generally a transient modification in motile activity. Some protists remain fixed to their substrate and perform contraction-relaxation cycles (some heliozoans and ciliates), the others are free-living, capable of swiming or “walking” (flagellates, amoebae, actinopods, most of the ciliates).


Rest Membrane Potential Membrane Excitability Contractile Vacuole Amoeboid Movement Rapid Contraction 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Amos, W. B., Routledge, L. M., and Yew, F. F., 1975, Calcium-binding proteins in a vorticellid contractile organelle, J. Cell Sci. 19:203–213.PubMedGoogle Scholar
  2. Andrivon, C., 1988, Membrane control of ciliary movement in ciliates, Biol. Cell. 63:133–142.PubMedCrossRefGoogle Scholar
  3. Braatz-Shade, K., 1978, Effects of various substances and cell shape, motile activity and membrane potential in Amoeba proteus, Acta Protozool. 17:163–176.Google Scholar
  4. Bonini, N. M., Gustin, M. C., and Nelson, D. L., 1986, Regulation of ciliary motility by membrane potential in Paramecium: A role for cyclic AMP, Cell Motility and the Cytoskeleton 6:256–272.PubMedCrossRefGoogle Scholar
  5. Butler, R. D., and McCrohan, C. R., 1987, Stimulus-response coupling in the contraction of tentacles of the suctorian protozoon Helioptoya erhardi, J. Cell Sci. 88:121–127.Google Scholar
  6. Cachon, J., and Cachon, M., 1982, Induction of unusual structures after a microtubule disassembly in the protozoan Sticholonche zanclea, in: Microtubules in Microorganisms, pp. 325–339 (P. Cappuccinelli and N. R. Morris, eds.), Marcel Dekker, Inc., New York, Basel.Google Scholar
  7. Cohen, J., Garreau de Loubresse, N., and Beisson, J., 1984, Actin microfilaments in Paramecium: localization and role in intracellular movements, Cell Motility 4:443–468.PubMedCrossRefGoogle Scholar
  8. Davidson, L. A., 1975, Studies of the actinopods Heterophils marina and Ciliophrys marina: Energetics and structural analysis of their contractile axopodia, general ultrastructure and phylogenetic relationships, Ph.D. thesis, University of California at Berkeley, pp. 1-163.Google Scholar
  9. de Brabander, M. J., Geuens, G., Nuiden, R., Willebords, R., and de Mey, J., 1981, Taxol induces the assembly of free microtubules in living cells and blocks the organizing capacity of the centrosomes and kinetochores, Proc. Natl. Acad. Sci. USA 78:608–5612.CrossRefGoogle Scholar
  10. de Peyer J. E., and Deitmer, J. W., 1980, Divalent cations as charge carriers during two functionally different membrane currents in the ciliates Stylonychia, J. exp. Biol. 1988:73–89.Google Scholar
  11. de Peyer J. E., and Machemer, H., 1977, Membrane excitability in Stylonychia. Properties of the two-peak regenerative calcium response, J. Comp. Physiol. 121:15–32.CrossRefGoogle Scholar
  12. Deitmer, J. W., 1981, Voltage and time characteristics of the potassium mechanoreceptor current in the ciliate Stylonychia, J. Comp. Physiol. 141:173–182.CrossRefGoogle Scholar
  13. Deitmer, J. W., 1986, Voltage dependence of two inward currents carried by calcium and barium in the ciliate Stylonychia mytilus, J. Physiol. (Lond.) 380:551–574.Google Scholar
  14. Detmers, P. A., Carboni, J. M., and Condeelis, J., 1985, Localization of actin in Chlamydomonas using antiactin and NBD phallacidin, Cell Motility 5:415–430.PubMedCrossRefGoogle Scholar
  15. Dryl, S., Demar-Gervais, C., and Kubalski, A., 1982, Contribution to studies on the role of external cations in excitability of marine ciliate Fabrea satina, Acta Protozoologica 21:55–59.Google Scholar
  16. Dustin, P., 1984, in: Microtubules (P. Dustin, ed.), Springer Verlag, Berlin, Heidelberg, New York.CrossRefGoogle Scholar
  17. Eckert, R., and Brehm, P., 1979, Ionic mechanisms of excitation in Paramecium, Ann. Rev. Biophys. Bioeng. 8:353–383.CrossRefGoogle Scholar
  18. Eckert, R., Naitoh, Y., and Friedman, K., 1972, Sensory mechanisms in Paramecium. I. Two components of the electric response to mechanical stimulation of the anterior surface, J. exp. Biol. 56:683–694.PubMedGoogle Scholar
  19. Eckert, R., Naitoh, Y., and Machemer, H., 1976, Calcium in the bioelectric and motor functions of Paramecium, in: Calcium in Biological Systems, pp. 233–255 (Duncan, ed.), Cambridge University Press, London.Google Scholar
  20. Eckert, R., and Sibaoka, T., 1967, Bioelectric regulation of tentacle movement in a dinoflagellate, J. exp. Biol. 47:433–446.PubMedGoogle Scholar
  21. Edds, K. T., 1981, Cytoplasmic streaming in a heliozoan, Biosystems 14:371–376.PubMedCrossRefGoogle Scholar
  22. Evans, R. L., McCrohan, C. R., and Butler, R. D., 1988, Tentacle contraction in Heliophrya erhardi (Suctoria): the role of inositol phospholipid metabolites and cyclic nucleotide in stimulus-response coupling, Exp. Cell Res. 177:382–390.PubMedCrossRefGoogle Scholar
  23. Evans, R. L., Butler, R. D., McCrohan, C. R., and Cuthbertson, K. S. R., 1989, Control of tentacle contraction in suctorian protozoa, Intern. Congr. Protozool. 10–17 July 1989, Tsukuba, Japan. S5-5, p. 53.Google Scholar
  24. Fabczac, S. and Fabczac, H. (1988), The resting and action membrane potentials of the ciliate Blepharisma japonicum, Acta Protozool. 27:117–124.Google Scholar
  25. Febvre, J., 1971, Le myonème d’acanthaire: Essai d’interprétation ultrastructurale et cinétique, Protistologica 7:379–391.Google Scholar
  26. Febvre, J., 1981, The myoneme of the acantharia (Protozoa): A new model of cellular motility, Biosystems 14:327–336.PubMedCrossRefGoogle Scholar
  27. Febvre, J., and Febvre-Chevalier, C., 1982, Motility processes in acantharia (Protozoa). I. Cinematographic and cytological study of the myonemes. Evidence for a helix-coil of the constituent filaments, Biol. Cell 44:283–304.Google Scholar
  28. Febvre, J., and Febvre-Chevalier, C., 1989, Motility processes in acantharia (Protozoa). III. Calcium regulation of the contraction-relaxation cycles of in vivo myonemes, Biol. Cell 67(2), in press.Google Scholar
  29. Febvre-Chevalier, C., 1973, Un nouveau type d’association des microtubules axopodiaux chez les héliozoaires, Protistologica 9:35–43.Google Scholar
  30. Febvre-Chevalier, C., 1980, Behaviour and cytology of Actinocoryne contractais nov. gen. nov. sp. A new stalked heliozoan (Centrohelidia). Comparison with the other related genera, J. Mar. Biol. Ass. UK. 60:909–928.CrossRefGoogle Scholar
  31. Febvre-Chevalier, C., 1981, Preliminary study of the motility processes in the stalked heliozoan Actinocoryne contractilis, Biosystems 14:337–343.PubMedCrossRefGoogle Scholar
  32. Febvre-Chevalier, C., 1987, Ultrastructure et critères taxonomiques. Excitabilité et contractilité cellulaire d’héliozoaires marins (Protozoa, Actinopoda), Thèse Doctorat Es-Sciences, Office National des Thèses, Grenoble.Google Scholar
  33. Febvre-Chevalier, C., Bilbaut, A., Bone, Q., and Febvre, J., 1986, Sodium-calcium action potential associated with contraction in the heliozoan Actinocoryne contractilis, J. exp. Biol. 122:177–192.Google Scholar
  34. Febvre-Chevalier, C., and Febvre, J., 1980, Cytophysiology of motility in a pedunculated heliozoan, Film, SFRS, Paris.Google Scholar
  35. Febvre-Chevalier, C., and Febvre, J., 1986, Motility mechanisms in the actinopods (Protozoa): A review with particular attention to axopodial contraction-extension and movement of nonactin filament systems, Cell Motility and the Cytoskeleton 6:198–208.CrossRefGoogle Scholar
  36. Fukui, Y., and Yumura, S., 1986, Acto-myosin dynamics in chemotactic amoeboid movement of Dictyostelium, Cell Motility and the Cytoskeleton 6:662–673.CrossRefGoogle Scholar
  37. Gibbons, I. R., 1989, Microtubule-based motility: An overview of a fast-moving field, in: Cell Movement, vol. 1, The dynein ATPases, pp. 3–22 (F. D. Warner, P. Satir, and I. R. Gibbons, eds.), Alan R. Liss, New York.Google Scholar
  38. Goodenough, U. W., and Heuser, J. E., 1989, Structure of the soluble and in situ ciliary dyneins visualized by quick-freeze deep-etch microscopy, in: Cell Movement, vol. 1, The dynein ATPases, pp. 121–140 (F. D. Warner, P. Satir, and I. R. Gibbons, eds.), Alan R. Liss, New York.Google Scholar
  39. Götz von Olenhusen, K-, and Wohlfarth-Bottermann, K. E., 1979, Effects of caffeine and D2O on persistence and de novo generation of intrinsic oscillatory contraction automaticity in Physarum, Cell Tissue. Res. 197:479–499.PubMedGoogle Scholar
  40. Hausmann, K., Linnenbach, M., and Patterson, D. J., 1983, The effect of taxol on microtubular arrays. In vivo effects on heliozoan axonemes, J. Ultrastr. Res. 82:212–220.CrossRefGoogle Scholar
  41. Hinrichsen, R. D. and Saimi, Y., 1984, A mutation that alters properties of Ca2+ channels in Paramecium tetrauretia, J. Physiol. (Lond.) 351:397–410.Google Scholar
  42. Hinrichsen, R. D., Saimi, Y., Ramanathan, R., Burgess-Cassler, A., and Kung, C., 1985, A genetic and biochemical analysis of behavior, in: Sensing and Response in Microorganisms, pp. 147–157 (M. Eisenbach, and M. Balaban, ed.), Elsevier, New York.Google Scholar
  43. Huang, B., and Pitelka, D. R., 1973, The contractile process in the ciliate Stentor coeruleus. The role of microtubules and filaments, J. Cell Biol. 57:704–728.PubMedCrossRefGoogle Scholar
  44. Huitorel, P., 1988, From cilia and flagella to intracellular motility and back again: A review of a few aspects of microtubule-based motility, Biol. Cell. 63:249–258.PubMedCrossRefGoogle Scholar
  45. Kamada, T., 1934, Some observations on potential differences across the ectoplsm membrane of Paramecium, J. exp. Biol. 11:94–102.Google Scholar
  46. Kiehart, D. P., and Pollard, T. D., 1984, Inhibition of Acanthomoeba actomyosin-II ATPase activity and mechanochemical function by monoclonal antibodies, J. Cell Biol. 99:1024–1033.PubMedCrossRefGoogle Scholar
  47. Kim, I. H., Prusti, R. K., Song, P. S., Haeder, D. P., and Haeder, M., 1984, Phototaxis and Photophobic response in Stentor coeruleus. Action spectrum and role of calcium fluxes, Biochim. Biophys. Acta. 799:298–304.PubMedCrossRefGoogle Scholar
  48. Kinosita, H., 1954, Electric potentials and ciliary response in Opalina, J. Fac. Sci. Tokyo Univ. IV 7:1–14.Google Scholar
  49. Kinosita, H., Dryl, S., and Naitoh, Y., 1964, Changes in the membrane potential and the response to stimuli in Paramecium, J. Fac. Sci. Tokyo Univ. IV 10:291–301.Google Scholar
  50. Kubalski, A., 1987, The effects of tetraethylammonium on the excitability of marine ciliate Fabrea salina, Acta Protozoologica 26:135–144.Google Scholar
  51. Kung, C., Chang, S. Y., Satow, Y., Van Houten, J., and Hansma, H., 1975, Genetic dissection of behaviour in Paramecium, Science 188:898–904.PubMedGoogle Scholar
  52. Kung, C., and Saimi, Y., 1982, The physiological basis of taxes in Paramecium, Ann. Rev. Physiol. 44:519–534.CrossRefGoogle Scholar
  53. Kung, C., and Saimi, Y., 1985, Ca2+ channnels of Paramecium. A multidisciplinary study, in: Current Topics in Membrane and Transport, 23, pp. 46-66, Acad. Press.Google Scholar
  54. Machemer, H., and Deitmer, J. W., 1987, From structure to behaviour Stylonychia as a model system for cellular physiology, Progress in Protistology 2:213–330.Google Scholar
  55. Marsland, D., Tilney, L. G., and Hirshfield, M., 1971, Stabilizing effect of heavy water on the microtubular components and needle-like form of the heliozoan axopods. A pressure, temperature analysis, J. Cell. Physiol. 77:187–194.PubMedCrossRefGoogle Scholar
  56. Matsuoka, T., and Shigenaka, Y., 1986, Elongation and contraction of Blepharisma evoked by mechanical or light stimulation, Arch. Protistenk. 131:85–94.CrossRefGoogle Scholar
  57. McFadden, G. I., Schulze, D., Surek, B., Salisbury, J. L., and Melkonian, M., 1987, Basal body reorientation mediated by Ca2+-modulated contractile protein, J. Cell Biol. 105:903–912.PubMedCrossRefGoogle Scholar
  58. Moreton, R. B., and Amos, W. B., 1979, Electrical recording from the contractile ciliate Zoothamnium geniculatum Ayrton, J. exp. Biol. 83:159–167.Google Scholar
  59. Naitoh, Y., 1968, Ionic control of the reversal response of cilia in Paramecium caudatum. A calcium hypothesis, J. Gen. Physiol. 51:85–103.PubMedCrossRefGoogle Scholar
  60. Naitoh, Y., 1982, Protozoa, in: Electric Conduction and Behaviour in “Simple” Invertebrates, pp. 1–48 (G. A. B. Shelton, ed.), Clarendon Press, Oxford.Google Scholar
  61. Naitoh, Y., Eckert, R., 1968, Electrical properties of Paramecium caudatum: all or none electrogenesis, Z. Vergl. Physiologie 61:453–472.CrossRefGoogle Scholar
  62. Naitoh, Y., Eckert, R., 1973, Sensory mechanisms in Paramecium. II. Ionic basis of the hyperpolarizing mechanoreceptor potential, J. exp. Biol. 59:53–65.Google Scholar
  63. Naitoh, Y., Eckert, R., and Friedman, K., 1972, A regenerative calcium response in Paramecium, J. exp. Biol. 56:667–681.PubMedGoogle Scholar
  64. Naitoh, Y., and Oami, K., 1989, Bioelectric control of the tentacle movement in the dinoflagellate Noctiluca, Ville Intern. Congr. Protozool., July 10–17, 1989, Tsukuba, Japan.Google Scholar
  65. Nawata, T., and Sibaoka, T., 1986 Membrane potential controlling the initiation of feeding in the marine dinoflagellate Noctiluca, Zool., Sci., Tokyo 3:49–58.Google Scholar
  66. Nichols, K. M., and Rikmenspoel, R., 1978, Control of flagellar motility in Euglena and Chlamydomonas. Microinjection of EDTA, EGTA, Mn2+ and Zn2+, Exp. Cell Res. 116:33–40.CrossRefGoogle Scholar
  67. Nishi, T., Gotow, T., and Kobayashi, M., 1988, Changes in electrical connections during cell fusion in the heliozoan Echinosphaerium akame, J. exp. Biol. 135:183–191.Google Scholar
  68. Nishi, T., Kobayashi, M., and Shigenaka, Y., 1986, Membrane activity and its correlation with vacuolar contraction in the heliozoan Echinosphaerium, J. Exp. Zool. 239:175–182.CrossRefGoogle Scholar
  69. Nuccitelli, R., Poo, M. N., and Jaffe, L. F., 1977, Relations between amoeboid movement and membrane-controlled electrical currents, J. Gen. Physiol. 69:743–763.PubMedCrossRefGoogle Scholar
  70. Oami, K., Sibaoka, T., Naitoh, Y., 1988, Tentacle regulating potentials in Noctiluca miliaris. Their generation sites and ionic mechanisms, J. Comp. Physiol. 162:179–186.CrossRefGoogle Scholar
  71. Ogura, A., and Machemer, H., 1980, Distribution of mechanoreceptor channels in the Paramecium surface membrane, J. Comp. Physiol. 135:233–242.CrossRefGoogle Scholar
  72. Otter, T., 1989, Calmodulin and the control of flagellar movement, in: Cell Movement, vol. 1, The dynein ATPases, pp. 281–298 (F. D. Warner, P. Satir, and I. R. Gibbons, eds.), Alan R. Liss, New York.Google Scholar
  73. Pollard, T. D., and Weihing, R. R., 1974, Actin and myosin and cell movement, CRC Crit. Rev. Biochem. 2:1–65.PubMedCrossRefGoogle Scholar
  74. Roberts, T. M., 1987, Invited review: Fine (2-5 nm) filaments: New types of cytoskeletal structures, Cell Motility and the Cytoskeleton 8:130–142.PubMedCrossRefGoogle Scholar
  75. Routledge, L. M., Amos, W. B., Yew, F. F., and Weis-Fogh, T., 1976, New calcium-binding contractile proteins, in: Cell Motility, pp. 93-114 (B. R. Goldman, T., Pollard, and J. Rosenbaum, eds.), Cold Spring Harbor Laboratory.Google Scholar
  76. Saimi, Y., and Kung, C., 1988, Ion channels of Paramecium, yeast and Escherichia coli, in: Current Topics in Membrane and Transport, 33, pp. 1–11, Acad. Press, New York, London.Google Scholar
  77. Salisbury, J. L., Baron, A., Surek, B., Melkonian, M., 1984, Stiated flagellar roots: Isolation and partial characterization of a calcium modulated contractile organelle, J. Cell Biol. 99:962–970.PubMedCrossRefGoogle Scholar
  78. Satir, P., 1984, The generation of ciliary motion, J. Protozool. 31:8–12.PubMedGoogle Scholar
  79. Satir, P., 1989, Structural analysis of the dynein cross-bridge cycle, in: Cell Movement, vol. 1, The dynein ATPases, pp. 219–234 (F. D. Warner, P. Satir, and L.R. Gibbons, eds.), Alan R. Liss, New York.Google Scholar
  80. Satir, B. H., Garofalo, R. S., Gilligan, D. M., and Maihle, N. J., 1980, Possible functions of calmodulin, in: Calmodulin and Cell Functions (D. N. Watterson and F. F. Vicenzi), Ann. New York Acad. Sci. 356:83–91.CrossRefGoogle Scholar
  81. Satow, Y., 1978, Internal calcium concentration and potassium permeability in Paramecium. J. Neurobiol. 9:81–91.PubMedCrossRefGoogle Scholar
  82. Schliwa, M., 1986, The cytoskeleton, in: Cell Biology Monographs, 13, pp. 1–323, Springer Verlag, Vienne, New York.Google Scholar
  83. Schmidt, J. A., and Eckert, R., 1976, Calcium couples flagellar reversal to photostimulation in Chlamydomonas reinhardtii, Science 262:713–715.Google Scholar
  84. Shigenaka, Y., Roth, L. E., and Pihlaja, D. J., 1971, Microtubules in the heliozoan axopodium. III. Degradation and reformation after dilute urea treatment, J. Cell Sci. 8:127–151.PubMedGoogle Scholar
  85. Shigenaka, Y., Tadokoro, Y., Kaneda, M., 1975, Microtubules in protozoan cells. I. Effects of light metal ions on the heliozoan microtubules and their kinetic analysis. Ann. Zool. Jap. 48:227–241.Google Scholar
  86. Shiono, H., Hara, R., and Asai, H., 1980, Spontaneous membrane potential changes associated with the zoid and vacuolar contraction in Vorticella convallaria, J. Protozool. 27:83–87.Google Scholar
  87. Sibaoka, T., and Eckert, R., 1967, An electrophysiological study of the tentacle-regulating potential in Noctiluca, J. exp. Biol. 47:447–459.PubMedGoogle Scholar
  88. Small, E. B., and Lynn, D. H., 1985, Phylum Ciliophora Doflein, 1901, in: An Illustrated Guide to the Protozoa, pp. 393-575 (J. J. Lee, S. H. Hutner, and E. C. Bovee, eds.), Society of Protozoologists, Lawrence.Google Scholar
  89. Stephens, R. E., and Stommel, E. W., 1989, Role of cyclic adenosin monophosphate in ciliary and flagellar motility, in: Cell Movement, vol. 1, The dynein ATPases, pp. 299–316 (F. D. Warner, P. Satir, and I. R. Gibbons, eds.), Alan R. Liss, New York.Google Scholar
  90. Tasaki, I., and Kamiya, N., 1964, A study of electrophysiological properties of carnivorous amoebae, J. Cell Comp. Physiol. 63:365–380.CrossRefGoogle Scholar
  91. Taylor, D. L., 1976, Motile model systems of amoeboid movement, in: Cell Motility, pp. 797-821 (R. Goldman, T. Pollard, and J. Rosenbaum, eds), CSH Conferences on Cell Proliferation. V. III.Google Scholar
  92. Taylor, D. L., and Condeelis, J. S., 1979, Cytoplasmic structure and contractility in amoeboid cells, Intern. Rev. Cytol. 56:57–144.CrossRefGoogle Scholar
  93. Thiery, R., Klein, R., and Tatischeff, I., 1988, Phorbol 12-myristate 13-acetate modulates the cAMP-induced light-scattering response of a Dictyostelium discoideum cell population, FEB. 149-153.Google Scholar
  94. Tilney, L. J., 1968, Studies on the microtubules in heliozoa. IV The effect of colchicine on the formation and maintenance of the axopodia and the redevelopement of pattern in Actinosphaerium nucleofilum (Barrett), J. Cell Sci. 3:549–562.PubMedGoogle Scholar
  95. Tilney, L. J., Hiramoto, Y., and Marsland, D., 1966, Studies on the microtubules in Heliozoa. III. A pressure analysis of the role of these structures of the formation and maintenance of the axopodia of Actinosphaerium nucleofilum (Barrett), J. Cell Biol. 29:77–86.PubMedCrossRefGoogle Scholar
  96. Tilney, L. J., and Porter, K., 1967, Studies on the microtubules in the heliozoa. II. The effect of low temperature on these structures in the formation and maintenance of the axopodia, J. Cell Biol. 34:327–358.PubMedCrossRefGoogle Scholar
  97. Wood, D. C., 1970, Electrophysiological studies of the protozoan Stentor coeruleus, J. Neurobiol. 1:363–377.PubMedCrossRefGoogle Scholar
  98. Wood, D. C., 1982, Membrane permeabilities determining resting, action and mechanoreceptor potentials in Stentor coeruleus, J. Comp. Physiol. 146:537–540.CrossRefGoogle Scholar
  99. Wood, D. C., 1988a, Habituation in Stentor. A response-dependent process, J. Neurosci. 8:2248–2253.PubMedGoogle Scholar
  100. Wood, D. C., 1988b, Habituation in Stentor produced by mechanoreceptor channel modification, J. Neurosci. 8:2254–2258.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 1989

Authors and Affiliations

  • Colette Febvre-Chevalier
    • 1
  • André Bilbaut
    • 2
  • Jean Febvre
    • 1
  • Quentin Bone
    • 3
  1. 1.U.R.A 671Laboratoire de Biologie Cellulaire MarineVillefranche-sur-MerFrance
  2. 2.URA 651Laboratoire de Cytologie ExperimentaleNice-CedexFrance
  3. 3.The Marine LaboratoryCitadel Hill, PlymouthUK

Personalised recommendations