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Ultrastructure of spermatozoa in the seminal receptacle of the liver fluke Opisthorchis felineus (Rivolta, 1884)

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Abstract

The spermatozoon ultrastructure in the seminal receptacle of the liver fluke Opisthorchis felineus (Digenea, Opisthorchiidae), the agent of human opisthorchiasis endemic to Russia and Eastern Europe, was examined. The bean-shaped seminal receptacle of O. felineus has a wall consisting of epithelial and muscle layers. Mature spermatozoa are located in the interior of the seminal receptacle, whereas vacuoles containing degenerating spermatozoa are detectable at the periphery. The mature spermatozoon of O. felineus has two axonemes of a 9 + “1” pattern, a nucleus, two mitochondria, a lamellar body, two bundles of parallel cortical microtubules and an external ornamentation of the plasma membrane in the anterior area of the sperm. The lamellar body is likely to be the third mitochondrion of a small size. The cytoplasm of the spermatozoon is filled with numerous electron-dense granules of storage polysaccharides. Additionally, the ultrastructural characteristics of the seminal receptacle and spermatozoa of O. felineus were compared to available published data on other trematode species. The functional roles of the observed structures of this spermatozoon are discussed.

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References

  • Bakhoum AJS, Bâ CT, Fournier-Chambrillon C, Torres J, Fournier P, Miquel J (2009) Spermatozoon ultrastructure of Euryhelmis squamula (Rudolphi, 1819) (Digenea, Opisthorchiodea, Heterophyidae), an intestinal parasite of Mustela vison (Carnivora, Mustelidae). Revista Ibero-Latinoamericana de Parasitología 1:37–45

    Google Scholar 

  • Bakker KE, Diegenbach PC (1972) The ultrastructure of spermatozoa of Aspidogaster conchicola Baer, 1826 (Aspidogastridae, Trematoda). Neth J Zool 23:345–346

    Article  Google Scholar 

  • Barker SC, Blair D, Garrett AR, Cribb TH (1993) Utility of the D1 domain of nuclear 28S rRNA for phylogenetic inference in the Digenea. Syst Parasitol 26:181–188

    Article  Google Scholar 

  • Blair D (1993) The phylogenetic position of the Aspidobothrea within the parasitic flatworms inferred from ribosomal RNA sequence data. Int J Parasitol 23:169–178

    Article  CAS  PubMed  Google Scholar 

  • Bray RA, Gibson DI, Jones A (2008) Keys to the Trematoda, vol 3. CABI Publishing and the Natural History Museum, Wallingford

    Google Scholar 

  • Burton PR (1972) Fine structure of the reproductive system of a frog lung fluke. III. The spermatozoon and its differentiation. J Parasitol 58:68–83

    Article  CAS  PubMed  Google Scholar 

  • Foata J, Quilichini Y, Marchand B (2007) Spermiogenesis and sperm ultrastructure of Deropristis Inflata Molin, 1859 (Digenea, Deropristidae), a parasite of Anguilla anguilla. Parasitol Res 101:843–852

    Article  PubMed  Google Scholar 

  • Fürst T, Duthaler U, Sripa B, Utzinger J, Keiser J (2012) Trematode infections: liver and lung flukes. Infect Dis Clin North Am 26:399–419. doi:10.1016/j.idc.2012.03.008

    Article  PubMed  Google Scholar 

  • Grebenshchikov VM, Nacheva LV (2007) Micromorphology of Opisthorchis felineus spermateca. Rossijskij parazitologicheskij zhurnal 1:11–13

    Google Scholar 

  • Jeong KH (1983) A study on the structure of Clonorchis sinensis, a liver fluke: IV. Probable functions of the Laurer’s canal. Korean J Parasitol 21:209–218

    Article  Google Scholar 

  • Jeong KH, Rim HJ (1984) A study on the fine structure of Clonorchis sinensis, a liver fluke. V. The mature spermatozoa. Korean J Parasitol 22:30–36

    Article  Google Scholar 

  • Justine JL (1995) Spermatozoal ultrastructure and phylogeny in the parasitic Platyhelminthes. Mem Mus Natl Hist Nat 166:55–86

    Google Scholar 

  • Justine JL, Mattei X (1982) Étude ultrastructurale de la spermiogenèse et du spermatozoïde d’un Plathelminthe: Gonapodasmius (Trematoda: Didymozoidae). J Ultra Res 79:350–365

    Article  CAS  Google Scholar 

  • Justine JL, Mattei X (1984) Ultrastructural observations on the spermatozoon, oocyte and fertilisation process in Gonupodasmius, a gonochoristic trematode (Trematoda: Digenea: Didymozoidae). Acta Zool 65:171–177. doi:10.1111/j.1463-6395.1984.tb00822.x

    Article  Google Scholar 

  • Justine JL, Lambert A, Mattei X (1985) Spermatozoon ultrastructure and phylogenetic relationships in the monogeneans (Platyhelminthes). Int J Parasitol 15:601–608

    Article  CAS  PubMed  Google Scholar 

  • Kacem H, Bakhoum AJ, Neifar L, Miquel J (2010) Spermiogenesis and spermatozoon ultrastructure of the digenean Neoapocreadium chabaudi (Apocreadiidae), a parasite of Balistes capriscus (Pisces, Teleostei). Parasitol Int 59:358–366. doi:10.1016/j.parint.2010.04.008

    Article  CAS  PubMed  Google Scholar 

  • Kang S, Sultana T, Loktev VB, Wongratanacheewin S, Sohn WM, Eom KS, Park JK (2008) Molecular identification and phylogenetic analysis of nuclear rDNA sequences among three opisthorchid liver fluke species (Opisthorchiidae: Trematoda). Parasitol Int 57:191–197. doi:10.1016/j.parint.2007.12.007

    Article  CAS  PubMed  Google Scholar 

  • King S, Scholz T (2001) Trematodes of the family Opisthorchiidae: a mini review. Korean J Parasitol 39:209–221

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Levron C, Ternengo S, Marchand B (2003) Ultrastructure of spermiogenesis and the spermatozoon of Helicometra fasciata (Digenea, Opecoelidae), a parasite of Labrus merula (Pisces, Teleostei). Acta Parasitol 48:255–264

    Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004a) Spermiogenesis and sperm ultrastructure of Poracanthium furcatum (Digenae, Opecoelidae), a parasite of Mullus surmuletus (Pisces, Teleostei). Acta Parasitol 49:190–200

    Google Scholar 

  • Levron C, Ternengo S, Marchand B (2004b) Ultrastructure of spermiogenesis and the spermatozoon of Monorchis parvus Looss, 1902 (Digenea, Monorchiidae), a parasite of Diplodus annularis (Pisces, Teleostei). Parasitol Res 93:102–110

    Article  PubMed  Google Scholar 

  • Levron C, Suchanová E, Poddubnaya L, Oros M, Scholz T (2009) Spermatological characters of the aspidogastrean Aspidogaster limacoides Diesing, 1835. Parasitol Res 105:77–85. doi:10.1007/s00436-009-1367-3

    Article  PubMed  Google Scholar 

  • Levron C, Miquel J, Oros M, Scholz T (2010) Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biol Rev Camb Philos Soc 85:523–543. doi:10.1111/j.1469-185X.2009.00114.x

    PubMed  Google Scholar 

  • Miquel J, Nourrisson C, Marchand B (2000) Ultrastructure of spermiogenesis and the spermatozoon of Opecoeloides furcatus (Trematoda, Digenea, Opecoelidae), a parasite of Mullus barbatus (Pisces, Teleostei). Parasitol Res 86:301–310

    Article  CAS  PubMed  Google Scholar 

  • Miquel J, Fournier-Chambrillon C, Fournier P, Torres J (2006) Spermiogenesis and spermatozoon ultrastructure of the cranial digenean Troglotrema acutum (Leuckart, 1842). J Parasitol 92:441–453

    Article  PubMed  Google Scholar 

  • Ndiaye PI, Miquel J, Feliu C, Marchand B (2003) Ultrastructure of spermiogenesis and spermatozoa of Notocotylus neyrai González Castro, 1945 (Digenea, Notocotylidae), intestinal parasite of Microtus agrestis (Rodentia: Arvicolidae) in Spain. Invertebr Reprod Dev 43:105–115. doi:10.1080/07924259.2003.9652529

    Article  Google Scholar 

  • Ndiaye PI, Miquel J, Bâ CT, Marchand B (2004) Spermiogenesis and ultrastructure of the spermatozoon of the liver fluke Fasciola gigantica Cobbold, 1856 (Digenea: Fasciolidae), a parasite of cattle in Senegal. J Parasitol 90:30–40

    Article  PubMed  Google Scholar 

  • Ndiaye PI, Diagne PM, Sène A, Bakhoum AJ, Miquel J (2012) Ultrastructure of the spermatozoon of the digenean Lecithocladium excisum (Rudolphi, 1819) (Hemiuroidea: Hemiuridae), a parasite of marine teleosts in Senegal. Folia Parasitol 59:173–178

    Article  PubMed  Google Scholar 

  • Olson PD, Tkach VV (2005) Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Adv Parasitol 60:165–243

    Article  PubMed  Google Scholar 

  • Olson PD, Cribb TH, Tkach VV, Bray RA, Littlewood DT (2003) Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). Int J Parasitol 33:733–755

    Article  CAS  PubMed  Google Scholar 

  • Orido Y (1988) Ultrastructure of spermatozoa of the lung fluke, Paragonimus ohirai (Trematoda: Troglotrematidae), in the seminal receptacle. J Morphol 196:333–343

    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 Leningrad 221:61–78

    Google Scholar 

  • Quilichini Y, Foata J, Marchand B (2007a) Ultrastructural study of the spermatozoon of Nicolla testiobliquum (Digenea, Opecoelidae) parasite of brown trout Salmo trutta (Pisces, Teleostei). Parasitol Res 101:1295–1301

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Marchand B (2007b) Ultrastructural study of the spermatozoon of Pronoprymna ventricosa (Digenea, Baccigerinae), parasite of the twaite shad Alosa fallax Lacepede (Pisces, Teleostei). Parasitol Res 101:1125–1130

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Orsini A, Marchand B (2007c) Spermiogenesis and spermatozoon ultrastructure of Nicolla wisniewskii (Digenea, Opecoelidae), an intestinal parasite of brown trout Salmo trutta (Pisces, Teleostei). J Parasitol 93:469–478

    Article  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Justine JL, Bray RA, Marchand B (2010) Spermatozoon ultrastructure of Aponurus laguncula (Digenea: Lecithasteridae), a parasite of Aluterus monoceros (Pisces: Teleostei). Parasitol Int 59:22–28. doi:10.1016/j.parint.2009.06.007

    Article  CAS  PubMed  Google Scholar 

  • Quilichini Y, Foata J, Justine JL, Bray RA, Marchand B (2011) Spermatozoon ultrastructure of Gyliauchen sp. (Digenea: Gyliauchenidae), an intestinal parasite of Siganus fuscescens (Pisces: Teleostei). Biol Bull 221:197–205

    CAS  PubMed  Google Scholar 

  • Rees GF (1979) The ultrastructure of the spermatozoon and spermiogenesis in Cryptocotyle lingua (Digenea: Heterophyidae). Int J Parasitol 9:405–419

    Article  Google Scholar 

  • Rohde K, Watson NA, Cribb T (1991) Ultrastructure of sperm and spermatogenesis of Lobatostoma manteri (Trematoda, Aspidogastrea). Int J Parasitol 21:409–419

    Article  CAS  PubMed  Google Scholar 

  • Rohde K, Hefford C, Ellis JT, Baverstock PR, Johnson AM, Watson NA, Dittmann S (1993) Contributions to the phylogeny of platyhelminthes based on partial sequencing of 18S ribosomal DNA. Int J Parasitol 23:705–724

    Article  CAS  PubMed  Google Scholar 

  • Saijuntha W, Sithithaworn P, Wongkham S, Laha T, Chilton NB, Petney TN, Barton M, Andrews RH (2008) Mitochondrial DNA sequence variation among geographical isolates of Opisthorchis viverrini in Thailand and Lao PDR, and phylogenetic relationships with other trematodes. Parasitology 135:1479–1486

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schatten H, Chakrabarti A (2000) Fertilisation in invertebrates. In: Tarín JJ, Cano A (eds) Fertilisation in protozoa and metazoan animals: cellular and molecular aspects. Springer, Berlin, Heidelberg, pp 27–87

    Chapter  Google Scholar 

  • Seck MT, Marchand B, Bâ CT (2007) Ultrastructure of spermiogenesis and the spermatozoon of Paramphistomum microbothrium [Fischoeder 1901] (Digenea: Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 101:653–662

    Article  PubMed  Google Scholar 

  • Seck MT, Marchand B, Bâ CT (2008) Spermiogenesis and sperm ultrastructure of Cotylophoron cotylophorum (Trematoda, Digenea, Paramphistomidae), a parasite of Bos taurus in Senegal. Parasitol Res 103(1):157–166. doi:10.1007/s00436-008-0944-1

    PubMed  Google Scholar 

  • Skryabin KI (1947) Trematodes of animals and man, vol 1. Izdatel’stvo Akademii Nauk SSSR, Moscow

    Google Scholar 

  • Smyth JD, Halton DW (1983) The physiology of Trematodes, 2nd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Thaenkham U, Blair D, Nawa Y, Waikagul J (2012) Families Opisthorchiidae and Heterophyidae: are they distinct? Parasitol Int 61:90–93. doi:10.1016/j.parint.2011.06.004

    Article  CAS  PubMed  Google Scholar 

  • Wannaprapo S, Tesana S, Arunyanat C, Kanla P, Chaijaroonkhanarak W (2008) Morphological features of the testes of the adult liver fluke, Opisthorchis viverrini. Srinagarind Med J 23:346–352

    Google Scholar 

  • Watson NA, Rohde K (1991) Ultrastructure of spermatogenesis and sperm of Multicotyle purvisi (Plathelminthes, Aspidogastrea). Zoomorphology 110:347–356

    Article  Google Scholar 

  • Watson NA, Rohde K (1992) Ultrastructure of sperm and spermatogenesis of Rugogaster hydrolagi, Schell 1973 (Platyhelminthes, Trematoda, Aspidogastrea, Rugogastridae). Parasitol Res 78:516–524

    Article  CAS  PubMed  Google Scholar 

  • Yossepowitch O, Gotesman T, Assous M, Marva E, Zimlichman R, Dan M (2004) Opisthorchiasis from imported raw fish. Emerg Infect Dis 10:2122–2126

    Article  PubMed  Google Scholar 

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Acknowledgments

We cordially thank M. N. Lvova and Dr. A. V. Katokhin (IC&G SB RAS) for providing the live specimens of O. felineus. This work was supported by the Integration project of fundamental research of SB RAS (№19).

Ethical standards

The handling and care of M. auratus golden hamsters were conducted in strict accordance with the recommendations in the NIH Guide for the Care and Use of Laboratory Animals. The study protocol was approved by the Committee on the Ethics of Animal Experiments of the Institute of Cytology and Genetics SB RAS (permit number 7 of 19.11.2011).

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Correspondence to Elena Kiseleva.

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Zhukova, M.V., Mordvinov, V.A. & Kiseleva, E. Ultrastructure of spermatozoa in the seminal receptacle of the liver fluke Opisthorchis felineus (Rivolta, 1884). Parasitol Res 113, 1093–1101 (2014). https://doi.org/10.1007/s00436-013-3746-z

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