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Trematode reproduction in the molluscan host: an ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae)

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Abstract

The germinal mass in Himasthla elongata rediae was studied in detail using transmission electron microscopy. It was shown to be a specialized reproductive organ consisting of germinal cells at various maturation stages, supporting cells and stem cells. The germinal mass also contains early cercarial embryos emerging as a result of cleavage division of mature germinal cells. The stem cells that give rise to germinal cells have heterochromatin-rich nuclei with distinct nucleoli and scarce cytoplasm containing mainly free ribosomes and few mitochondria. The differentiating germinal cells undergo a growth, which is accompanied by an emergence of annulate lamellae and the nuage in their cytoplasm, a noticeable development of RER and Golgi apparatus and an increase in the number of mitochondria. The mitochondria form a large group at one of the cell poles. During differentiation, the nucleus and nucleolus of the germinal cell enlarge while the chromatin becomes gradually less condensed. The supporting tissue of the germinal mass is made up of cells connected by septate junctions. These supporting cells are distinctly different in cellular shape and nuclear ultrastructure. Their outgrowths form a tight meshwork housing stem cells, germinal cells and early cercarial embryos. The cytoplasm of the supporting cells in the mesh area is separated into fine parallel layers by labyrinthine narrow cavities communicating with the intercellular space. The supporting tissue contains differentiating and degenerating cells which indicates its renewal. The results of this ultrastructural study lend support to the hypothesis that the germinal cells of digeneans are germ line cells.

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References

  • Agata K (2008) Stem cells in planarian. In: Bosch TCG (ed) Stem cells: from Hydra to man. Springer, New York, pp 59–74

    Chapter  Google Scholar 

  • Allen WB, Nollen PM (1991) A comparative study of the regenerative processes in a trematode, Philophthalmus gralli, and a planarian, Dugesia dorotocephala. Int J Parasitol 21:441–447

    Article  CAS  PubMed  Google Scholar 

  • Ataev GL, Avanessjan AV, Loker ES, Dobrovolskij AA (2001a) The organization of the germinal material and dynamics of mother sporocyst reproduction in the genus Echinostoma (Trematoda: Echinostomatidae). Parazitologiya 35:307–319 (In Russian)

    CAS  Google Scholar 

  • Ataev GL, Dobrovolskij AA, Avanessjan AV, Loker ES (2001b) Germinal elements and their development in Echinostoma caproni and E. paraensei (Trematoda) miracidia. J Parasitol 87:1160–1164

    CAS  PubMed  Google Scholar 

  • Baguňà J (2012) The planarian neoblast: the rambling history of its origin and some current black boxes. Int J Dev Biol 56:19–37

    Article  PubMed  Google Scholar 

  • Bentley AG (1982) Tegumental repair in the adult trematode Ochetosoma aniarum. J Parasitol 68:1096–1104

    Article  Google Scholar 

  • Björkman N, Thorsell W (1964) On the ultrastructure of the ovary of the liver fluke (Fasciola hepatica L.). Z Parasitenkd 63:538–549

    Google Scholar 

  • Brehm K (2010) Echinococcus multilocularis as an experimental model in stem cell research and molecular host–parasite interaction. Parasitology 137:537–555

    Article  CAS  PubMed  Google Scholar 

  • Cheng TC, Bier JW (1972) Studies on molluscan schistosomiasis: an analysis of the development of the cercaria of Schistosoma mansoni. Parasitology 64:129–142

    Article  CAS  PubMed  Google Scholar 

  • Cifrian B, Martinez-Alos S, Gremini V (1993) Ultrastructural and cytochemical studies on the germarium of Dicrocoelium dendriticum (Plathelminthes, Digenea). Zoomorphology 113:165–171

    Article  Google Scholar 

  • Clark RB (1974) Interpretation of life history pattern in Digenea. Int J Parasitol 4:115–123

    Article  CAS  PubMed  Google Scholar 

  • Collins JJ, Wang B, Lambrus BG, Tharp ME, Iyer H, Newmark PA (2013) Adult somatic stem cells in the human parasite Schistosoma mansoni. Nature 494:476–479

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cort WW, Ameel DJ, Van der Woude A (1954) Germinal development in the sporocysts and rediae of the digenetic trematodes. Exp Parasitol 3:185–255

    Article  CAS  PubMed  Google Scholar 

  • Dobrovolskij AA, Galaktionov KV, Muhamedov GK, Sinha BK, Tihomirov IA (1983) Parthenogenetic generations of trematodes. Tr Leningr Obshestva Estestvoispytatelei 82:1–108 (in Russian)

    Google Scholar 

  • Dobrovolskij AA, Ataev GL (2003) The nature of reproduction of trematodes rediae and sporocysts. In: Combes C, Jourdane J (eds) Taxonomy ecology and evolution of metazoan parasites, vol I. PUP, Perpignan, pp 249–272

    Google Scholar 

  • Dunn TS, Dang PH, Hanna REB, Nisami WA (1992) Embryological development of the cercarial tegument of Paramphistomum epiclitum in the planorbid snail, Indoplanorbis exustus. J Helminthol 66:243–254

    Article  Google Scholar 

  • Extavour CG, Akam M (2003) Mechanisms of germ cell specification across the metazoans: epigenesis and preformation. Development 130:5869–5884

    Article  CAS  PubMed  Google Scholar 

  • Fried B, Awatramani R (1992) Light and scanning electron microscopical observations of the daughter rediae of Echinostoma trivolvis (Trematoda). Parasitol Res 78:257–259

    Article  CAS  PubMed  Google Scholar 

  • Galaktionov KV, Dobrovolskij AA (2003) The biology and evolution of trematodes. Kluwer Academic, Dordrecht, London

    Book  Google Scholar 

  • Gibson DI (1987) Questions in digenean systematics and evolution. Parasitology 95:429–460

    Article  PubMed  Google Scholar 

  • Grant WC, Harkema R, Muse KE (1977) Ultrastructure of Pharyngostomoides procyonis Harkema 1942 (Diplostomatidae). II. The female reproductive system. J Parasitol 63:1019–1030

    Article  CAS  PubMed  Google Scholar 

  • Halton DW, Stranock SD, Hardcastle A (1974) Vitelline cell development in monogenean parasites. Z Parasitenkd 45:45–61

    Article  CAS  PubMed  Google Scholar 

  • Halton DW, Stranock SD, Hardcastle A (1976) Fine structural observations on oocyte development in monogeneans. Parasitology 73:13–23

    Article  CAS  PubMed  Google Scholar 

  • Hay ED, Coward SJ (1975) Fine structure studies on the planarian, Dugesia. I. Nature of the “neoblast” and other cell types in noninjured worms. J Ultrastruct Res 50:1–21

    Article  CAS  PubMed  Google Scholar 

  • Higuchi S, Hayashi T, Hori I, Shibata N, Sakamoto H, Agata K (2007) Characterization and categorization of fluorescence activated cell sorted planarian stem cells by ultrastructural analysis. Dev Growth Differ 49:571–581

    Article  PubMed  Google Scholar 

  • Hori I (1992) Cytological approach to morphogenesis in the planarian blastema I. Cell behavior during blastema formation. J Submicrosc Cytol Pathol 24:75–84

    Google Scholar 

  • Hoskin GP (1975) Light and electron microscopy of the host-parasite interface and histopathology of Nassarius obsoletus infected with rediae of Himasthla quissetensis. Ann N Y Acad Sci 266:497–512

    Article  CAS  PubMed  Google Scholar 

  • Isakova NP (2011) Germinal mass of the rediae of Trematoda. Parazitologiya 45:358–366 (In Russian)

    CAS  Google Scholar 

  • Klag J, Niewiadomska K, Czubaj A (1997) Ultrastructural studies on the sporocyst wall of Diplostomum pseudospathaceum Niewiadomska, 1984 (Digenea, Diplostomidae). Int J Parasitol 27:919–929

    Article  CAS  PubMed  Google Scholar 

  • Køie M (1982) The redia, cercaria and early stages of Aporocotyle simplex Odhner, 1900 (Sanguinicolidae)–a digenetic trematode which has a polychaete annelid as the only intermediate host. Ophelia 21:115–145

    Article  Google Scholar 

  • Køie M, Petersen ME (1988) A new annelid intermediate host (Lanassa nordenskioeldi Malmgren, 1866) (Polychaeta: Terebellidae) for Aporocotyle sp. and a new final host family (Pisces: Bothidae) for Aporocotyle simplex Odhner, 1900 (Digenea: Sanguinicolidae). J Parasitol 74:499–502

    Article  Google Scholar 

  • Koulish S (1965) Ultrastructure of differentiating oocytes in the trematode Gorgoderina attenuata. I. The “nucleolus-like” cytoplasmic body and some lamellar membrane systems. Dev Biol 12:248–268

    Article  CAS  PubMed  Google Scholar 

  • Krejci KG, Fried B (1994) Light and scanning electron microscopic observations of the eggs, daughter rediae, cercariae, and encysted metacercariae of Echinostoma trivolvis and E. caproni. Parasitol Res 80:42–47

    Article  CAS  PubMed  Google Scholar 

  • Lumsden RD (1965) Macromolecular structure of glycogen in some cyclophyllidean and trypanorhynch cestodes. J Parasitol 51:501–515

    Article  CAS  PubMed  Google Scholar 

  • Meuleman EA, Holzmann PJ, Peet RC (1980) The development of daughter sporocysts inside the mother sporocyst of Schistosoma mansoni with special reference to the ultrastructure of the body wall. Z Parasitenkd 61:201–212

    Article  CAS  PubMed  Google Scholar 

  • Morozova KN, Gubanova NV, Kiseleva EV (2005) Structural organization and possible functions of annulate lamellae. Tsitologiya 47:667–678 (In Russian)

    CAS  Google Scholar 

  • Orido Y, Takamure A, Akamatsu T, Takashima Y (1994) Ultrastructure of the ootype of the lung fluke Paragonimus ohirai (Digenea, Troglotrematidae) in mated and single-infection worms. Parasitol Res 80:307–311

    Article  CAS  PubMed  Google Scholar 

  • Pan SC-T (1980) The fine structure of the miracidium of Schistosoma mansoni. J Invert Pathol 36:307–372

    Article  CAS  Google Scholar 

  • Pearson JC (1972) A phylogeny of life cycle patterns of the Digenea. Adv Parasitol 10:153–189

    Article  CAS  PubMed  Google Scholar 

  • Pinheiro J, Maldonado AJ, Attias M, Lanfredi RM (2004) Morphology of the rediae of Echinostoma paraensei (Trematoda: Echinostomatidae) from its intermediate host Lymnaea columella (Mollusca, Gastropoda). Parasitol Res 93:171–177

    Article  CAS  PubMed  Google Scholar 

  • Podvyaznaya IM (1990) The morphology and ultrastructure of the female reproductive system of Prosthodendrium ascidia (Trematoda, Lecithodendriidae). Proc Zool Inst USSR Acad Sci 221:61–78 (in Russian)

    Google Scholar 

  • Podvyaznaya IM (2003) Ultrastructural studies of the female reproductive system in a parasite of bats Allassogonoporus amphoraeformis (Digenea: Allassogonoporidae). Parazitologiya 37:387–393 (in Russian)

    Google Scholar 

  • Podvyaznaya IM (2007) An ultrastructural study of reproduction in the sporocysts of Prosorhynchoides gracilescens (Digenea: Bucephalidae). Parasitol Res 101:35–42

    Article  CAS  PubMed  Google Scholar 

  • Podvyaznaya IM, Galaktionov KV (2012) Morpho-functional specialization of the branching sporocyst of Prosorhynchoides borealis Bartoli, Gibson & Bray, 2006 (Digenea, Bucephalidae). J Helminthol 86:173–184

    Article  CAS  PubMed  Google Scholar 

  • Popiel I, Irving DL, Basch PF (1985) Wound healing in the trematode Schistosoma. Tissue Cell 17:69–77

    Article  CAS  PubMed  Google Scholar 

  • Reuter M, Kreshchenko N (2004) Flatworm asexual multiplication implicates stem cells and regeneration. Can J Zool 82:334–356

    Article  Google Scholar 

  • Rieger RM, Legniti A, Ladurer P, Reiter D, Asch E, Salvenmoser W, Schurmann W, Peter R (1999) Ultrastructure of neoblasts in microturbellaria: significance for understanding stem cells in free-living Platyhelminthes. Invert Reprod Dev 35:127–140

    Article  Google Scholar 

  • Rink JC (2013) Stem cell systems and regeneration in planaria. Dev Genes Evol 223:67–84

    Article  PubMed Central  PubMed  Google Scholar 

  • Robinson RD, Halton DW (1982) Fine structural observations on spermatogenesis in Corrigia vitta (Trematoda: Dicrocoeliidae). Z Parasitenkd 68:53–72

    Article  Google Scholar 

  • Saffman EE, Lasko P (1999) Germline development in vertebrates and invertebrates. Cell Mol Life Sci 55:1141–1163

    Article  CAS  PubMed  Google Scholar 

  • Sato K, Shibata N, Orii H, Amikura R, Sakurai T, Agata K, Kobayashi S, Watanabe K (2006) Identification and origin of the germline stem cells as revealed by the expression of nanos-related gene in planarians. Dev Growth Differ 48:615–628

    Article  CAS  PubMed  Google Scholar 

  • Shibata N, Rouhana L, Agata K (2010) Cellular and molecular dissection of pluripotent adult somatic stem cells in planarians. Develop Growth Differ 52:27–41

    Article  CAS  Google Scholar 

  • Toledo R, Muñoz-Antoli C, Fried B (2007) The use of echinostomes to study host-parasite relationships between larval trematodes and invertebrate and cold-blooded vertebrate hosts. Parasitol Res 100:1177–1185

    Article  PubMed  Google Scholar 

  • Valkounová J, Zdárská Z, Nasincová V (1989) Ultrastructural observations on the redia of Echinostoma revolutum (Froelich, 1802). Folia Parasitol 36:25–30

    PubMed  Google Scholar 

  • Wang B, Collins JJ, Newmark PA (2013) Functional genomic characterization of neoblast-like stem cells in larval Schistosoma mansoni. eLife. doi:10.7554/eLife.00768

    Google Scholar 

  • Whitfield PJ, Evans NA (1983) Parthenogenesis and asexual multiplication among parasitic platyhelminths. Parasitology 86:121–160

    Article  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the Russian Foundation for Basic Research (grant no 13-04-00875). The authors are deeply grateful to Mr. AE Tenison for his technical assistance.

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Correspondence to Irina M. Podvyaznaya.

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Podvyaznaya, I.M., Galaktionov, K.V. Trematode reproduction in the molluscan host: an ultrastructural study of the germinal mass in the rediae of Himasthla elongata (Mehlis, 1831) (Digenea: Echinostomatidae). Parasitol Res 113, 1215–1224 (2014). https://doi.org/10.1007/s00436-014-3760-9

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