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Actin pegs and ultrastructure of presumed sensory receptors of Beroë (Ctenophora)

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Summary

We have investigated the actin content and ultrastructure of two kinds of presumed sensory projections on the lip epidermis of beroid ctenophores. Transmission electron microscopy showed that conical pegs contain a large bundle of densely packed, parallel microfilaments. Rhodamine-phalloidin brightly stained the pegs, confirming that they contain filamentous actin. Epidermal cells with actin pegs also bear a single long cilium with an onion-root structure, previously described as arising from a different type of cell. The actin peg and onion-root cilium project side-by-side, defining a polarized axis of the cell which is shared by neighboring cells. The onion-root body is surrounded by a flattened membranes sac which lies immediately below the plasma membrane. The perimeter of the membrane sac is encircled by aggregates of dense material. An extra layer of dense material is found along the side of the membrane sac facing the peg; this material often makes direct contact with the adjacent actin filament bundle. Cells with actin pegs and onion-root cilia synapse onto adjacent neurites and secretory gland cells, indicating that one or both types of projections are sensory elements. Since the feeding responses of beroids are reported to depend on chemical and tactile stimuli to the lips, the cells bearing pegs and cilia may function as both mechanoreceptors and chemoreceptors, that is, as double sensory receptors.

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References

  • Anderson PAV (1984) The electrophysiology of single smooth muscle cells isolated from the ctenophore Mnemiopsis. J Comp Physiol [B] 154:257–268

    Google Scholar 

  • Bilbaut A, Hernandez-Nicaise M-L, Leech CA, Meech RW (1988a) Membrane currents that govern smooth muscle contraction of a ctenophore. Nature 331:533–535

    Google Scholar 

  • Bilbaut A, Meech RW, Hernandez-Nicaise M-L (1988b) Isolated giant smooth muscle fibres in Beroë ovata: Ionic dependence of action potential reveals two distinct types of fibre. J Exp Biol 135:343–362

    Google Scholar 

  • Chun C (1880) Der Ctenophoren des Golfes von Neapel, und der angrenzenden Meeres-Abschnitte. Flora und Fauna des Golfes von Neapel vol 1. Engelmann, Leipzig

    Google Scholar 

  • Corey DP, Hudspeth AJ (1980) Mechanical stimulation and micromanipulation with piezoelectric bimorph elements. J Neurosci Methods 3:183–202

    Google Scholar 

  • DeRosier DJ, Tilney LG (1984) The form and function of actin. In: Shay JW (ed) Cell and muscle motility, vol 5. Plenum, New York, pp 139–169

    Google Scholar 

  • Eimer T (1880) Ueber Tastapparate bei Eucharis multicornis. Arch Mikr Anat 17:342–345

    Google Scholar 

  • Franc J-M (1970) Evolutions et interactions tissulaires au cours de la régénération des levres de Beroë ovata. Cahiers Biol Mar 11:57–76

    Google Scholar 

  • Heider K (1927) Vom Nervensystem der Ctenophoren. Z Morph Oekol Tiere 9:638–678

    Google Scholar 

  • Hernandez-Nicaise M-L (1973) The nervous system of ctenophores. III. Ultrastructure of synapses. J Neurocytol 2:249–263

    Google Scholar 

  • Hernandez-Nicaise M-L (1974) Ultrastructural evidence for a sensory-motor neuron in Ctenophora. Tissue Cell 6:43–47

    Google Scholar 

  • Hernandez-Nicaise M-L (1976) Evidence for neural control of muscles in ctenophores. In: Mackie GO (ed) Coelenterale ecology and behaviour. Plenum, New York, pp 513–522

    Google Scholar 

  • Hernandez-Nicaise M-L, Amsellem J (1980) Ultrastructure of the giant smooth muscle fiber of the ctenophore Beroë ovata. J Ultrastruct Res 72:151–168

    Google Scholar 

  • Hernandez-Nicaise M-L, Mackie GO, Meech RW (1980) Giant smooth muscle cells of Beroë. Ultrastructure, innervation, and electrical properties. J Gen Physiol 75:79–105

    Google Scholar 

  • Hernandez-Nicaise M-L, Bilbaut A, Malaval L, Nicaise G (1982) Isolation of functional giant smooth muscle cells from an invertebrate: structural features of relaxed and contracted fibers. Proc Natl Acad Sci USA 79:1884–1888

    Google Scholar 

  • Hernandez-Nicaise M-L, Nicaise G, Malaval L (1984) Giant smooth muscle fibers of the ctenophore Mnemiopsis leydii: ultrastructural study of in situ and isolated cells. Biol Bull 167:210–228

    Google Scholar 

  • Hertwig R (1880) Ueber den Bau der Ctenophoren. Jena Z Naturw 14:393–457

    Google Scholar 

  • Horridge GA (1965a) Relations between nerves and cilia in ctenophores. Am Zool 5:357–375

    Google Scholar 

  • Horridge GA (1965b) Non-motile sensory cilia and neuromuscular junctions in a ctenophore independent effector organ. Proc R Soc Lond [Biol] 162:333–350

    Google Scholar 

  • Horridge GA (1966) Pathways of co-ordination in ctenophores. In: Rees WJ (ed) The cnidaria and their evolution. Symp Zool Soc Lond 16:247–266

  • Horridge GA (1971) Primitive examples of gravity receptors and their evolution. In: Gordon SA, Cohen MJ (eds) Gravity and the organism, University of Chicago Press, Chicago, pp 203–221

    Google Scholar 

  • Horridge GA (1974) Recent studies on the Ctenophora. In: Muscatine L, Lenhoff HM (eds) Coelenterate biology. Academic Press, New York, pp 439–468

    Google Scholar 

  • Horridge GA, Mackay B (1964) Neurociliary synapses in Pleurobrachia (Ctenophora). Quart J Microsc Sci 105:163–174

    Google Scholar 

  • Hudspeth AJ (1989) How the ear's works work. Nature341:397–404

    Google Scholar 

  • Hufnagel LA, Kass-Simon G (1988) Functional anatomy of nematocyte innervation in battery cell complexes of the Hydra tentacle. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts, Academic Press, New York, pp 519–529

    Google Scholar 

  • Mackie GO, Mills CE, Singla CL (1988) Structure and function of the prehensile tentilla of Euplokamis (Ctenophora, Cydippida). Zoomorphol 107:319–337

    Google Scholar 

  • Moss AG, Tamm SL (1986) Electrophysiological control of ciliary motor responses in the ctenophore Pleurobrachia. J Comp Physiol [A] 158:311–330

    Google Scholar 

  • Moss AG, Tamm SL (1987) A calcium regenerative potential controlling ciliary reversal is propagated along the length of ctenophore comb plates. Proc Natl Acad Sci USA 84:6476–6480

    Google Scholar 

  • Nagel W (1893) Versuche zur Sinnesphysiologie von Beroë ovata und Carmarina hastata. Pflügers Arch Ges Physiol 54:165–188

    Google Scholar 

  • Nakamura S, Tamm SL (1985) Calcium control of ciliary reversal in ionophore-treated and ATP-reactivated comb plates of ctenophores. J Cell Biol 100:1447–1454

    Google Scholar 

  • Pantin CFA (1942) The excitation of nematocysts. J Exp Biol 19:294–310

    Google Scholar 

  • Parker GH, Van Alstyne MA (1932) The control and discharge of nematocysts, especially in Metridium and Physalia. J Exp Zool 63:329–344

    Google Scholar 

  • Pollard TD, Cooper JA (1986) Actin and actin-binding proteins. A critical evaluation of mechanisms and functions. Annu Rev Biochem 55:987–1035

    Google Scholar 

  • Sleigh MA (1972) Features of ciliary movement of the ctenophores Beroë, Pleurobrachia and Cestus. In: Clark RB, Wotton R (eds) Essays on hydrobiology. University Press, Exeter, pp 119–136

    Google Scholar 

  • Swanberg N (1974) The feeding behavior of Beroë ovata. Mar Biol 24:69–76

    Google Scholar 

  • Tamm SL (1973) Mechanisms of ciliary coordination in ctenophores. J Exp Biol 59:231–245

    Google Scholar 

  • Tamm SL (1980) Cilia and ctenophores. Oceanus 23:50–59

    Google Scholar 

  • Tamm SL (1982) Ctenophores. In: Shelton GAB (ed) Electrical conduction and behaviour in ‘simple’ invertebrates. University Press, Oxford, pp 266–358

    Google Scholar 

  • Tamm SL (1983) Motility and mechanosensitivity of macrocilia in the ctenophore Beroë. Nature 305:430–433

    Google Scholar 

  • Tamm SL (1984) Mechanical synchronization of ciliary beating within comb plates of ctenophores. J Exp Biol 113:401–408

    Google Scholar 

  • Tamm SL (1988a) Calcium activation of macrocilia in the ctenophore Beroë. J Comp Physiol 163:23–31

    Google Scholar 

  • Tamm SL (1988b) Iontophoretic localization of the Ca-sensitive sites controlling activation of ciliary beating in macrocilia of Beroë: the ciliary rete. Cell Motil 11:126–138

    Google Scholar 

  • Tamm SL (1989) Control of reactivation and microtubule sliding by calcium, strontium, and barium in detergent-extracted macrocilia of Beroë. Cell Motil 12:104–112

    Google Scholar 

  • Tamm SL, Moss AG (1985) Unilateral ciliary reversal and motor responses during prey capture by the ctenophore Pleurobrachia. J Exp Biol 114:443–461

    Google Scholar 

  • Tamm SL, Tamm S (1981) Ciliary reversal without rotation of axonemal structures in ctenophore comb plates. J Cell Biol 89:495–509

    Google Scholar 

  • Tamm SL, Tamm S (1985) Visualization of changes in ciliary tip configuration caused by sliding displacement of microtubules in macrocilia of the ctenophore Beroë. J Cell Sci 79:161–179

    Google Scholar 

  • Tamm SL, Tamm S (1987) Massive actin bundle couples macrocilia to muscles in the ctenophore Beroë. Cell Motil Cytoskel 7:116–128

    Google Scholar 

  • Tamm SL, Tamm S (1989a) Calcium sensitivity extends the length of ATP-reactivated ciliary axonemes. Proc Natl Acad Sci USA 86:6987–6991

    Google Scholar 

  • Tamm S, Tamm SL (1989b) Extracellular ciliary axonemes associated with the surface of smooth muscle cells of ctenophores. J Cell Sci 94:713–724

    Google Scholar 

  • Tamm SL, Tamm S (1990) Jellies with jaws. MBL Science 4:28–29

    Google Scholar 

  • Thorington GU, Hessinger DA (1988a) Control of cnida discharge. I. Evidence for two classes of chemoreceptor. Biol Bull 174:163–171

    Google Scholar 

  • Thorington GU, Hessinger DA (1988b) Control of discharge: factors affecting discharge of cnidae. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 233–253

    Google Scholar 

  • Watson GM, Hessinger DA (1987) Receptor-mediated endocytosis of a chemoreceptor involved in triggering the discharge of cnidae in a sea anemone tentacle. Tissue Cell 19:747–755

    Google Scholar 

  • Watson GM, Hessinger DA (1988) Localization of a purported chemoreceptor involved in triggering cnida discharge in sea anemones. In: Hessinger DA, Lenhoff HM (eds) The biology of nematocysts. Academic Press, New York, pp 255–272

    Google Scholar 

  • Westfall JA (1970a) Ultrastructure of synapses in a primitive coelenterate. J Ultrastruct Res 32:237–246

    Google Scholar 

  • Westfall JA (1970b) The nematocyte complex in a hydromedusan, Gonionemus vertens. Z Zellforsch 110:457–470

    Google Scholar 

Download references

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  1. Marine Biological Laboratory, Boston University Marine Program, 02543, Woods Hole, MA, USA

    Signhild Tamm & Sidney Tamm

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  1. Signhild Tamm
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  2. Sidney Tamm
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Tamm, S., Tamm, S. Actin pegs and ultrastructure of presumed sensory receptors of Beroë (Ctenophora). Cell Tissue Res 264, 151–159 (1991). https://doi.org/10.1007/BF00305733

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