Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Serotonin immunoreactivity in a highly enigmatic metazoan phylum, the pre-nervous Dicyemida

Abstract

Dicyemida are simply organized metazoans with a long axial cell surrounded by a layer of ciliated peripheral cells. Stem cells and propagates develop inside the cytoplasm of the axial cell. Two types of propagates exist, asexually formed vermiform embryos and sexually derived infusoriform larvae, neither of which, however, develop by gastrulation. Thus, Dicyemida lack all traits typical of common metazoa and represent a pre-nervous state of organization. In this study, immunofluorescence and immunoelectron microscopy have been used to investigate the presence of a serotonin-like molecule in adults and larvae of Dicyema typus and Dicyemennea antarcticensis. Generally, in the adults of both species, the main immunoreactive structures are confined either to small vesicles inside the peripheral cells or to prominent vesicles in the axial cell, the latter vesicles apparently playing a role during the differentiation of the stem cells and the development of the propagates. In all stages, faint immunoreactivity can be observed over the surface membrane and the ciliary apparatus and over the heterochromatic blocks in the nuclei. Surprisingly, in the infusoriform larva, striking immunoreactivity occurs in the vesicles of the capsule cells covering the urn cells, which contain germinal cells. These vesicles might represent stores used in a later life phase of the animal. The results suggest that, in the pre-nervous Dicyemida, serotonin in its ancestral form may function as a hormone regulating essential developmental and morphogenetic processes.

This is a preview of subscription content, log in to check access.

Fig. 1 Fig. 2 Fig. 3 Fig. 4
Fig. 5 Fig. 6 Fig. 7 Fig. 8 Fig. 9

References

  1. Aiello E (1974) Cilia and flagella. Academic Press, London

  2. Beneden E van (1876) Recherches sur les Dicyémides. Bull Acad Roy Belg 41:1160–1205

  3. Brizzi G, Blum JJ (1970) Effect of growth conditions on serotonin content of Tetrahymena pyriformis. J Protozool 17:553–555

  4. Buckland-Nicks J, Hodgson AN (2000) Fertilization in Callochiton castaneus (Mollusca). Biol Bull 199:59–67

  5. Busch H (1974) The cell nucleus. Academic Press, New York

  6. Buznikov GA, Nikitina L, Galanov AY, Malchenko L, Trubnikova OB (1993) The control of oocyte maturation in the starfish and amphibians by serotonin and its antagonists. Int J Dev Biol 37:363–364

  7. Buznikov GA, Shmukler YB, Lauder JM (1996) From oocyte to neuron: do neurotransmitters function in the same way throughout development? Cell Mol Neurobiol 16:533–599

  8. Buznikov GA, Lambert HW, Lander JM (2001) Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 305:177–186

  9. Cavalier-Smith T (1993) Kingdom protozoa and its 18 phyla. Microbiol Rev 57:953–994

  10. Cerda J, Reich G, Wallace RA, Selman K (1998) Serotonin inhibition of steroid-induced meiotic maturation in the teleost Fundulus heteroclitus: role of cyclic AMP and protein kinases. Mol Reprod Dev 49:333–341

  11. Csaba G, Kapa E, Cserhalmi M (1975) Hormone receptor studies on frog macrophage cells by means of histamine, serotonin and indole acetic acid. Endokrinologie 65:219–223

  12. Csaba G, Sudár F, Ubornyák L (1983) Comparative study of the internalization and nuclear localization of amino acid type hormones in Tetrahymena and rat lymphocytes. Exp Clin Endocrinol 82:61–67

  13. Czaker R (2000) Extracellular matrix (ECM) components in a very primitive animal, the dicyemid mesozoan Kantharella antarctica. Anat Rec 259:52–59

  14. Dodson EO (1956) A note on the systematic position of the mesozoa. Syst Zool 5:37–40

  15. Fong PP, Kyozuka K, Abdelghani H, Hardege JD, Ram L (1994) In vivo and in vitro induction of germinal vesicle breakdown in a freshwater bivalve, the zebra mussel Dreissena polymorpha (Pallas). J Exp Zool 269:467–474

  16. Freire-Garabal M, Nunez MJ, Balboa J, Lopez-Delgado P, Gallego R, Garcia-Caballero T, Fernandez-Roel MD, Brenlla J, Rey-Mendez M (2003) Serotonin upregulates the activity of phagocytes through 5-HT1A receptors. Br J Pharmacol 139:457–463

  17. Fujii K, Takeda N (1988) Phylogenetic detection of serotonin immunoreactive cells in the central nervous system of invertebrates. Comp Biochem Physiol 89C:233–239

  18. Furuya H, Tsuneki K, Hoshida Y (1997) Fine structure of dicyemid mesozoans with special reference to cell junctions. J Morphol 231:297–305

  19. Green CR, Bergquist PR (1979) Cell membrane specializations in the Porifera. In: Levi C, Boury-Esnault N (ed) Biologie des Spongiaires, vol 291. Colloque Int CNRS, Paris, pp 233–237

  20. Hay-Schmidt A (2000) The evolution of the serotonergic nervous system. Proc R Soc Lond [Biol] 267:1071–1079

  21. Hori H, Osawa S (1987) Origin and evolution of organisms as deduced form 5S ribosomal RNA sequences. Mol Biol Evol 4:445–472

  22. Hyman LH (1940) The invertebrates, vol 1. McGraw-Hill, New York

  23. Katayama T, Wada H, Furuya H, Satoh N, Yamamoto M (1995) Phylogenetic position of the dicyemid mesozoa inferred from 18S rDNA sequences. Biol Bull 189:81–90

  24. Kobayashi M, Furuya H, Holland PWH (1999) Dicyemids are higher animals. Nature 401:762

  25. Korneliussen H (1976) 5-Hydroxytryptamine: autoradiographic evidence for uptake into fibroblast cell nuclei. Experientia 32:443–445

  26. Koshtoyants KS, Buznikov GA, Manukhin BN (1961) The possible role of 5HT in the motor activity of embryos of some marine gastropods. Comp Biochem Physiol 3:20–26

  27. Lapan EA, Morowitz HJ (1974) Characterization of mesozoan DNA. Exp Cell Res 83:143–151

  28. Lynn DH, Corliss JO (1991) Phylum Ciliophora. In: Harrison FW, Corliss JO (ed) Microscopic anatomy of invertebrates. I. Protozoa. Wiley-Liss, New York, pp 333–449

  29. Matsubara JA, Dudley PL (1976) Fine structural studies of the dicyemid mesozoan Dicyemmenea californica McConnaughey. J Parasitol 62:377–389

  30. McCauley DW (1997) Serotonin plays an early role in the metamorphosis of the hydrozoan Phialidium gregarium. Dev Biol 190:229–240

  31. McConnaughey BH (1951) The lifecycle of the dicyemid mesozoa. Univ Calif Publ Zool 55:295–336

  32. Murakami A (1983) Control of ciliary beat frequency in Mytilus. J Submicrosc Cytol 15:313–316

  33. Noto T, Yazaki K, Endoh H (2003) Developmentally regulated extrachromosomal circular DNA formation in the mesozoan Dicyema japonicum. Chromosoma 111:359–368

  34. Nouvel H (1947) Les Dicyémides. Arch Biol 58:54–220

  35. Nouvel H (1948) Les Dicyémides. 2e Partie: infusoriforme, tératology, spécifité du parasitisme, affinitiés. Arch Biol 59:147–223

  36. Ohama T, Kumazaki K, Hori H, Osawa S (1984) Evolution of multicellular animals as deduced from 5S ribosomal RNA-sequences: a possible early emergence of the mesozoa. Nucleic Acid Res 12:5101–5108

  37. Paparo AA (1986) Average ciliary beat in the oyster: response to photoperiod, pentylenetetrazole, salyrgan, serotonin and dopamine. Mar Behav Physiol 12:149–159

  38. Pawlowski J, Montoya-Burgos JI, Fahrni FJ, Wüest J, Zaninetti L (1996) Origin of the mesozoa inferred from 18S rRNA gene sequences. Mol Biol Evol 13:1128–1132

  39. Renaud F, Parisi E, Capasso A, De Prisco P (1983) On the role of serotonin and 5-methoxy-tryptamine in the regulation of cell division in sea urchin eggs. Dev Biol 98:37–46

  40. Ridley RK (1968) Electron microscopic studies on dicyemid mesozoa. I. Vermiform stages. J Parasitol 54:975–998

  41. Rodriguez N, Renaud FL (1980) On the possible role of serotonin in the regulation of regeneration of cilia. J Cell Biol 85:242–247

  42. Shmukler YB, Tosti E (2002) Serotonergic-induced ion currents in cleaving sea urchin embryos. Inverteb Reprod Dev 42:43–49

  43. Stricker SA, Smythe TL (2000) Multiple triggers of oocyte maturation in nemertean worms: the roles of calcium and serotonin. J Exp Zool 287:243–261

  44. Stunkard HW (1954) The life history and systematic relations of the mesozoa. Q Rev Biol 29:230–244

  45. Turlejski K (1996) Evolutionary ancient roles of serotonin: long-lasting regulation of activity and development. Acta Neurobiol Exp 56:619–636

Download references

Acknowledgements

The author is grateful to Ms. A. Ficenc, Ms. M. Steiner and Ms. E. Vanyek for their skilled technical assistance and to Ms. C. Farrenkopf and Ms. Mag. R. Schulz for their competent editorial cooperation.

Author information

Correspondence to Renate Czaker.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Czaker, R. Serotonin immunoreactivity in a highly enigmatic metazoan phylum, the pre-nervous Dicyemida. Cell Tissue Res 326, 843–850 (2006). https://doi.org/10.1007/s00441-006-0247-8

Download citation

Keywords

  • Serotonin
  • Immunofluorescence
  • Immunoelectron microscopy
  • Mesozoa
  • Dicyemida