Cell and Tissue Research

, Volume 379, Issue 1, pp 63–71 | Cite as

Hydra nematocysts in the flatworm Microstomum lineare: in search for alterations preceding their disappearance from the new host

  • Georg KrohneEmail author
Regular Article


Nematocysts are characteristic organelles of the phylum Cnidaria. The free-living Platyhelminth Microstomum lineare preys on Hydra oligactis and sequesters nematocysts. All nematocyst types become phagocytosed without adherent cytoplasm by intestinal cnidophagocytes. Desmoneme and isorhiza nematocysts disappear within 2 days after ingestion whereas cnidophagocytes containing the venom-loaded stenotele nematocysts migrate out of the intestinal epithelia through the parenchyma to the epidermis. Epidermally localized stenoteles are still able to discharge suggesting that this hydra organelle does preserve its physiological properties. Three to four weeks after ingestion, the majority of stenoteles disappear from M. lineare. To search for alterations of nematocysts that might precede their disappearance, flatworms were stained with acridine orange, a dye that binds to poly-γ-glutamic acid present in hydra nematocysts. The staining properties of all three nematocyst types were indistinguishable during the first 60 min after ingestion of hydra tissue whereas 15 h later, the majority of desmoneme and isorhiza had lost their stainability in striking contrast to stenoteles. In M. lineare inspected 2, 4 and 10 days after feeding, 20–40% of stenoteles had lost their stainability with acridine orange. Non-stained stenoteles had sizes similar to their stained counterparts but some of them were slightly deformed. The presented data indicate that acridine orange staining allows the detection of early alterations of all three ingested nematocyst types preceding their disappearance from M. lineare. Furthermore, they support the notion that the transport of venom-loaded stenoteles to the epidermis provides a strategy of excretion.


Nematocyst Kleptocnidae Hydra Microstomum lineare Acridine orange 



I am grateful to my former students Melanie Stiegler and Melanie Bunz who performed some preliminary experiments under my supervision. I am very grateful to Ulrich Scheer and Christian Stigloher for critically reading the manuscript.

Compliance with ethical standards

Conflict of interest

The author declares that there are no conflicts of interest.

Ethical approval

All applicable national and institutional guidelines for the care and use of animals were followed.


  1. Beckmann A, Xiao S, Müller JP, Mercadante D, Nüchter T, Kröger N, Langhojer F, Petrich W, Holstein TW, Benoit M, Gräter F, Özbek S (2015) A fast recoiling silk-like elastomer facilitates nanosecond nematocyst discharge. BMC Biol 13:3. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Berking S, Herrmann K (2006) Formation and discharge of nematocysts is controlled by a proton gradient across the cyst membrane. Helgol Mar Res 60:180–188. CrossRefGoogle Scholar
  3. Bode HR (1996) The interstital cell lineage of hydra: a stem cell system that arose early in evolution. J. Cell Sci 109:1155–1164Google Scholar
  4. Carré C, Carré D (1980) Les cnidocystes du cténophore Euchlora rubra (Kölliker 1853). Cah Biol Mar 21:221–226Google Scholar
  5. Conklin EJ, Mariscal RN (1977) Feeding behavior, ceras structure, and nematocyst storage in the Aeolid nudibranch, Spurilla neapolitana (Mollusca). Bull Mar Sci 27:658–667Google Scholar
  6. Goodheart JA, Bely AE (2016) Sequestration of nematocysts by divergent cnidarian predators: mechanism, function, and evolution. Invertebrate Biol 136:75–91CrossRefGoogle Scholar
  7. Goodheart JA, Bleidißel S, Schillo D, Strong EE, Ayres DL, Preisfeld A, Collins AG, Cummings MP, Wägele H (2018) Comparative morphology and evolution of the cnidosac in Cladobranchia (Gastropoda: Heterobranchia: Nudibranchia). Front Zool DOI.
  8. Greenwood PG (2009) Acquisition and use of nematocysts by cnidarian predators. Toxicon 54:1065–1070CrossRefGoogle Scholar
  9. Greenwood PG, Mariscal RN (1984) The utilization of cnidarian nematocysts by aeolid nudibranchs: nematocyst maintenance and release in Spurilla. Tissue & Cell 16:719–730CrossRefGoogle Scholar
  10. Grosvenor GH (1903) On the nematocysts of aeolids. Proc R Soc Lond 72:462–486Google Scholar
  11. Holstein T (1981) The morphogenesis of nematocytes in Hydra and Forskålia: an ultrastructural study. J Ultrastr Res 75:276–290CrossRefGoogle Scholar
  12. Holstein T, Tardent P (1984) An ultrahigh-speed analysis of exocytosis: nematocyst discharge. Science 223:830–833CrossRefGoogle Scholar
  13. Holstein TW, Benoit M, Gv H, Wanner G, David CN, Gaub HE (1994) Fibrous mini-collagens in hydra nematocysts. Science 265:402–404CrossRefGoogle Scholar
  14. Kälker H, Schmekel L (1976) Bau und Funktion des Cnidosacks der Aeolidoidea (Gastropoda Nudibranchia). Zoomorphologie 86:41–60CrossRefGoogle Scholar
  15. Karling TG (1966) On nematocysts and similar structures in turbellarians. Acta Zool Fenn 116:3–28Google Scholar
  16. Khalturin K, Anton-Erxleben F, Milde S, Plötz C, Wittlieb J, Hemmrich G, Bosch TCG (2007) Transgenic stem cells in hydra reveal an early evolutionary origin for key elements controlling self-renewal and differentiation. Devl Biol 309:32–44CrossRefGoogle Scholar
  17. Krohne G (2018) Organelle survival in a foreign organism: Hydra nematocysts in the flatworm Microstomum lineare. Eur J Cell Biol 97:289–299CrossRefGoogle Scholar
  18. Kurz EM, Holstein TW, Petri BM, Engel J, David CN (1991) Mini-collagens in hydra nematocytes. J Cell Bio 115:1159–1169CrossRefGoogle Scholar
  19. Martin CH (1908) The nematocyst of Turbellaria. Quart J Microsc Sci 52:261–277Google Scholar
  20. Mills CE, Miller RL (1984) Ingestion of a medusa (Aegina citrea) by the nematocyst-containing ctenophore Haeckelia rubra (formerly Euchlora rubra): phylogenetic implications. Mar Biol 78:215–221CrossRefGoogle Scholar
  21. Nüchter T, Benoit M, Engel U, Özbek S, Holstein TW (2006) Nanosecond-scale kinetics of nematocyst discharge. Curr Biol 16:R316–R318CrossRefGoogle Scholar
  22. Obermann D, Bickmeyer U, Wägele H (2012) Incorporated nematocysts in Aeolidiella stephanieae (Gastropoda, Opistobranchia, Aeolidoidea) mature by acidification shown by the pH sensitive fluorescing alkaloid Ageladine A. Toxicon 60:1108–1116CrossRefGoogle Scholar
  23. Östman C (2000) A guideline to nematocyst nomenclature and classification, and some notes on the systematic value of nematocysts. Sci Mar 64(Suppl. 1):31–46CrossRefGoogle Scholar
  24. Penney BK, LaPlante LH, Friedman JR, Torres MO (2010) A noninvasive method to remove kleptocnidae for testing their role in defense. J Molluscan Studies 76:296–298CrossRefGoogle Scholar
  25. Ruppert EE, Barnes RD (1994) Invertebrate zoology, sixth edn. Saunders, New YorkGoogle Scholar
  26. Szczepanek S, Cikala M, David CN (2002) Poly-γ-glutamate synthesis during formation of the nematocyst capsules in Hydra. J Cell Sci 115:745–751PubMedGoogle Scholar
  27. Tardent P, Holstein T (1982) Morphology and morphodynamics of the stenotele nematocyst of Hydra attenuata. Cell Tissue Res 224:269–290CrossRefGoogle Scholar
  28. Thompson TE, Bennett I (1969) Physalia nematocysts: utilized by mollusks for defense. Science 166:1532–1533CrossRefGoogle Scholar
  29. Thompson TE, Bennett I (1970) Observation on Australian Glaucidae (Mollusca: Opisthobranchia). Zool J Linnean Soc 49:187–197CrossRefGoogle Scholar
  30. Tursch A, Mercadante D, Tennigkeit J, Gräter F, Özbek S (2016) Minicollagen cysteine-rich domains encode distinct modes of polymerization to form stable nematocyst capsules. Sci Rep 6:25709. CrossRefPubMedPubMedCentralGoogle Scholar
  31. von Siebold CT (1848) Lehrbuch der vergleichenden Anatomie der wirbellosen Thiere. Veith & Comp, Berlin, pp 161–163Google Scholar
  32. Weber J (1990) Poly(γ-glutamic acid)s are the major constituents of nematocysts in Hydra (Hydrozoa, Cnidaria). J Biol Chem 265:9664–9669PubMedGoogle Scholar
  33. Weber J (1995) Novel tools for the study of development, migration and turnover of nematocytes (cnidarian stinging cells). J Cell Sci 108:403–412PubMedGoogle Scholar
  34. Werner B (1965) Die Nesselkapseln der Cnidaria, mit besonderer Berücksichtigung der Hydroida. I Klassifizierung und Bedeutung für die Systematik und Evolution Helgoländer wiss Meeresuntersuchungen 12:1–39CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Imaging Core Facility BiocenterUniversity of WürzburgWürzburgGermany

Personalised recommendations