New data on spermiogenesis and trepaxonematan axoneme in basal tapeworms (Cestoda, Caryophyllidea, Lytocestidae) parasitizing cyprinid fishes
Jazyk angličtina Země Velká Británie, Anglie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
31501467
PubMed Central
PMC6733933
DOI
10.1038/s41598-019-49312-9
PII: 10.1038/s41598-019-49312-9
Knihovny.cz E-zdroje
- MeSH
- axonema metabolismus MeSH
- Cestoda cytologie fyziologie ultrastruktura MeSH
- Cyprinidae parazitologie MeSH
- elektronová mikroskopie MeSH
- spermatogeneze * MeSH
- zvířata MeSH
- Check Tag
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Monozoic caryophyllidean cestodes, intestinal parasites of cyprinid fishes, represent a group of tapeworms with an unclear evolutionary history. As spermatology may provide phylogenetically important data, the spermiogenesis and ultrastructure of the mature spermatozoon have been investigated using an integrative approach combining transmission electron microscopy, cytochemistry and electron tomography in Khawia rossittensis (Szidat, 1937). The process of spermatid formation is accompanied by the presence of ultrastructural characters not described in traditional models of spermiogenesis, e.g., apical electron-dense material, the two striated roots situated unusually opposite each other, branching of typical striated roots, an intercentriolar body comprising five electron-dense and four electron-lucent layers, rotation of both free flagella and flagellar buds to the median cytoplasmic process at 90°, and a complete proximodistal fusion. The synchronous rotation of both flagellar buds and growing free flagella is an evolutionarily linked pattern favouring the hypothesis that the Caryophyllidea are not ancestral but are secondarily derived from polyzoic forms. Electron tomography analysis has revealed a unique feature of two helicoidal tubular structures in the central electron-dense core of the axoneme of mature spermatozoon. These data provide new insights into the architecture of the 9 + '1' axoneme, which is shared by male gametes of all trepaxonematan Platyhelminthes.
Faculty of Science University of South Bohemia České Budějovice Czech Republic
Institute of Parasitology Slovak Academy of Sciences Košice Slovak Republic
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Scholz, T. & Oros, M. Caryophyllidea van Benedenin Cams, 1863 in Planetary Biodiversity Inventory (2008–2017): Tapeworms from Vertebrate Bowels of the Earth (eds Caira, J. N. & Jensen, K.) 47–64 (University of Kansas, Natural History Museum, Special Publication No. 25, Lawrence, KS, USA, 2017).
Mackiewicz JS. Caryophyllidea (Cestoidea): molecules, morphology and evolution. Acta Parasitol. 2003;48:143–154.
Waeschenbach A, Webster BL, Littlewood DTJ. Adding resolution to ordinal level relationships of tapeworms (Platyhelminthes: Cestoda) with large fragments of mtDNA. Mol. Phyogenet. Evol. 2012;63:834–47. doi: 10.1016/j.ympev.2012.02.020. PubMed DOI
Caira, J. N. & Littlewood, D. T. J. Worms, Platyhelminthes in Encyclopedia of biodiversity (ed. Levin, S. A.) 437–469 (Academic, Waltham, 2013).
Justine Jean-Lou. Spermatozoa as Phylogenetic Characters for the Eucestoda. The Journal of Parasitology. 1998;84(2):385. doi: 10.2307/3284502. PubMed DOI
Justine, J. L. Spermatozoa as phylogenetic characters for the Platyhelminthes in Interrelationships of the Platyhelminthes (eds Littlewood, D. T. J. & Bray, R. A.) 231–238 (Taylor and Francis, London 2001).
Justine, J. L. Ultrastructure des spermatozoïdes et phylegénie des Neodermata in Taxonomy, ecology and evolution of metazoan parasites (eds Combes, C. & Jourdane, J.) 359–380 (PUP, Perpignan, 2003).
Bruňanská, M. Recent insights into spermatozoa development and ultrastructure in the Eucestoda in Human spermatozoa: maturation, capacitation and abnormalities (eds Lejeune, T. & Delvaux, P.) 327–354 (Nova Science Publishers, Inc., New York, 2010).
Levron C, Miquel J, Oros M, Scholz T. Spermatozoa of tapeworms (Platyhelminthes, Eucestoda): advances in ultrastructural and phylogenetic studies. Biol. Rev. 2010;85:523–543. doi: 10.1111/j.1469-185X.2009.00114.x. PubMed DOI
Bruňanská M, Nebesářová J, Oros M. Ultrastructural aspects of spermatogenesis, testes, and vas deferens in the parthenogenetic tapeworm Atractolytocestus huronensis Anthony, 1958 (Cestoda:Caryophyllidea), a carp parasite from Slovakia. Parasitol. Res. 2011;108:61–68. doi: 10.1007/s00436-010-2038-0. PubMed DOI
Matoušková M, Bílý T, Bruňanská M, Mackiewicz JS, Nebesářová J. Ultrastructural, cytochemistry and electron tomography analysis of Caryophyllaeides fennica (Schneider, 1902) (Cestoda: Lytocestidae) reveals novel spermatology characteristics in the Eucestoda. Parasitol. Res. 2018;117:3091–3102. doi: 10.1007/s00436-018-6001-9. PubMed DOI
Bruňanská M, Poddubnaya LG. Spermiogenesis in the caryophyllidean cestode Khawia armeniaca (Cholodkovski, 1915) Parasitol. Res. 2006;99:449–454. doi: 10.1007/s00436-006-0155-6. PubMed DOI
Bruňanská M. Spermatological characters of the caryophyllidean cestode Khawia sinensis Hsü, 1935, a carp parasite. Parasitol. Res. 2009;105:1603–1610. doi: 10.1007/s00436-009-1599-2. PubMed DOI
Yoneva A, Levron C, Ash A, Scholz T. Spermatological characters of monozoic tapeworms (Cestoda: Caryophyllidea), including first data on a species from the Indomalayan catfish. J. Parasitol. 2012;98:423–430. doi: 10.1645/GE-2794.1. PubMed DOI
Arafa SZ, Hamada SF. Spermatogenesis and sperm ultrastructure of the caryophyllidean cestode, Monobothrioides chalmersius (Woodland, 1924) Hunter, 1930. Egypt. J. Zool. 2004;43:49–70.
Ehlers, U. Phylogenetishes System der Platyhelminthes Verhandl Naturwissensch Vereins Hamburg27, 291–294 (1984).
Bruňanská M, Bílý T, Nebesářová J. Nippotaenia mogurndae Yamaguti et Myiata, 1940 (Cestoda, Nippotaeniidea): first data on spermiogenesis and sperm ultrastructure. Parasitol. Res. 2015;114:1443–1453. doi: 10.1007/s00436-015-4327-0. PubMed DOI
Thiéry JP. Mise en évidence des polysaccharides sur coupes fines en microscopie électronique. J. Microsc. 1967;6:987–1018.
Świderski, Z. Three types of spermiogenesis in cestodes in Proc 11th Int. Congr. Electr. Microsc. (eds Imura, T., Maruse, S. & Suzuki, T.) 2959–2960 (Kyoto 1986).
Bâ, C. T. & Marchand, B. Spermiogenesis, spermatozoa and phyletic affinities in the Cestoda in Advances in spermatozoal phylogeny and taxonomy (eds Jamieson, B. G. M., Ausie, J. & Justine, J. L.) 87–95 (Mém. Mus. natn. Hist. nat. (1995).
Miquel J, Świderski Z, Mackiewicz JS, Ibraheem MH. Ultrastructure of spermiogenesis in the caryophyllidean cestode Wenyonia virilis Woodland, 1923, with re-assessment of flagellar rotation in Glaridacris catostomi Cooper, 1920. Acta Parasitol. 2008;53:19–29. doi: 10.2478/s11686-008-0013-z. DOI
Gamil IS. Ultrastructural studies of the spermatogenesis and spermiogenesis of the caryophyllidean cestode Wenyonia virilis (Woodland, 1923) Parasitol. Res. 2008;103:777–785. doi: 10.1007/s00436-008-1040-2. PubMed DOI
Yoneva A, Levron C, Oros M, Orosová M, Scholz T. Ultrastructure of spermiogenesis and mature spermatozoon of Breviscolex orientalis (Cestoda: Caryophyllidea) Parasitol. Res. 2011;108:997–1005. doi: 10.1007/s00436-010-2144-z. PubMed DOI
Yoneva A, Levron C, Oros M, Orosová M, Scholz T. Spermiogenesis and spermatozoon ultrastructure of Hunterella nodulosa (Cestoda: Caryophyllidea), amonozoic parasite of suckers (Catostomidae) in North America. Folia Parasitol. 2012;59:179–186. doi: 10.14411/fp.2012.025. PubMed DOI
Bruňanská M, Kostič B. Revisiting caryophyllidean type of spermiogenesis in the Eucestoda based on spermatozoon differentiation and ultrastructure of Caryophyllaeus laticeps (Pallas, 1781) Parasitol. Res. 2012;110:141–149. doi: 10.1007/s00436-011-2463-8. PubMed DOI
Bruňanská M, Poddubnaya LG, Xylander WER. A reinvestigation of spermiogenesis in Amphilina foliacea (Platyhelminthes, Amphilinidea) Folia Parasitol. 2013;60:43–50. doi: 10.14411/fp.2013.006. PubMed DOI
Bruňanská M, Scholz T, Dezfuli B, Poddubnaya LG. Spermiogenesis and sperm ultrastructure of Cyathocephalus truncatus (Pallas, 1781) Kessler, 1868 (Cestoda: Spathebothriidea) J. Parasitol. 2006;92:884–892. doi: 10.1645/GE-718R1.1. PubMed DOI
Bruňanská M, Poddubnaya LG. Spermatological characters of the spathebothriidean tapeworm Didymobothrium rudolphii (Monticelli, 1890) Parasitol. Res. 2010;106:1435–1442. doi: 10.1007/s00436-010-1822-1. PubMed DOI
Levron C, Bruňanská M, Poddubnaya LG. Spermatological characters in Diphyllobothrium latum (Cestoda, Pseudophyllidea) J. Morphol. 2006;267:1110–1119. doi: 10.1002/jmor.10460. PubMed DOI
Levron C, Sitko J, Scholz T. Spermiogenesis and spermatozoon of the tapeworm Ligula intestinalis (Diphyllobothriidae): phylogenetic implications. J. Parasitol. 2009;95:1–9. doi: 10.1645/GE-1646.1. PubMed DOI
Levron C, Yoneva A, Kalbe M. Spermatological characters in the diphyllobothriidean Schistocephalus solidus (Cestoda) Acta Zool. 2013;94:240–247. doi: 10.1111/j.1463-6395.2011.00549.x. DOI
Yoneva A, Kuchta R, Scholz T. Spermiogenesis and sperm ultrastructure of two species of Duthiersia, parasites of monitors, with a review of spermatological characters in the Diphyllobothriidea (Cestoda) Zool. Anz. 2013;252:486–494. doi: 10.1016/j.jcz.2013.01.002. DOI
Bruňanská M, Nebesářová J, Scholz T, Fagerholm HP. Spermiogenesis in the pseudophyllid cestode Eubothrium crassum (Bloch, 1779) Parasitol. Res. 2001;87:579–588. doi: 10.1007/s004360100392. PubMed DOI
Levron C, Bruňanská M, Marchand B. Spermiogenesis and sperm ultrastructure of the pseudophyllidean cestode Triaenophorus nodulosus (Pallas, 1781) Parasitol. Res. 2005;98:26–33. doi: 10.1007/s00436-005-0009-7. PubMed DOI
Levron C, Bruňanská M, Poddubnaya LG. Spermatological characters of the pseudophyllidean cestode Bothriocephalus scorpii (Müller, 1776) Parasitol. Int. 2006;55:113–120. doi: 10.1016/j.parint.2005.11.055. PubMed DOI
Šípková L, Levron C, Freeman M, Scholz T. Spermiogenesis and spermatozoon of the tapeworm Parabothriocephalus gracilis (Bothriocephalidea): ultrastructural and cytochemical studies. Acta Parasitol. 2010;55:58–65. doi: 10.2478/s11686-010-0003-9. DOI
Šípková L, Levron C, Oros M, Justine JL. Spermatological characters of bothriocephalideans (Cestoda) inferred from an ultrastructural study on Oncodiscus sauridae and Senga sp. Parasitol. Res. 2011;109:9–18. doi: 10.1007/s00436-010-2215-1. PubMed DOI
Marigo AM, Delgado E, Torres J, Bâ CT, Miquel J. Spermiogenesis and spermatozoon ultrastructure of the bothriocephalidean cestode Clestobothrium crassiceps (Rudolphi, 1819), a parasite of the teleost fish Merluccius merluccius (Gadiformes: Merlucciidae) Parasitol. Res. 2012;110:19–30. doi: 10.1007/s00436-011-2446-9. PubMed DOI
Marigo AM, Levron C, Bâ CT, Miquel J. Ultrastructural study of spermiogenesis and the spermatozoon of the proteocephalidean cestode Barsonella lafoni de Chambrier et al., 2009, a parasite of the catfish Clarias gariepinus (Burchell, 1822) (Siluriformes, Clariidae) Zool. Anz. 2012;251:147–159. doi: 10.1016/j.jcz.2011.08.002. DOI
Olson PD, Poddubnaya LG, Littlewood DTJ, Scholz T. On the position of Archigetes and its bearing on the early evolution of the tapeworms. J. Parasitol. 2008;94:898–904. doi: 10.1645/GE-1456.1. PubMed DOI
Bruňanská M, Matoušková M, Nebesářová J, Mackiewicz JS, Poddubnaya LG. First ultrastructural and cytochemical data on the spermatozoon and its differentiation in progenetic and adult Archigetes sieboldi Leuckart, 1878 (Cestoda, Caryophyllidea, Caryophyllaeidae) Parasitol. Res. 2019;118:1205–1214. doi: 10.1007/s00436-019-06276-z. PubMed DOI
Marigo AM, Świderski Z, Bâ CT, Miquel J. Spermiogenesis and ultrastructure of the spermatozoon of the trypanorhynch cestode Aporhynchus menezesi (Aporhynchidae), a parasite of the velvet belly lanternshark Etmopterus spinax (Elasmobranchii: Etmopteridae) Folia Parasitol. 2011;58:69–78. doi: 10.14411/fp.2011.007. PubMed DOI
Świderski Z, Mackiewicz JS. Ultrastructure of spermatogenesis and spermatozoa of the caryophyllidean cestode Glaridacris catostomi Cooper, 1920. Acta Parasitol. 2002;47:83–104.
Mokhtar-Maamouri F. Étude en microscopie électronique de la spermatogénèse et du spermatozoïde de Phyllobothrium gracile Wedl, 1855 (Cestoda, Tetraphyllidea, Phyllobothriidae) Z. Parasitenkd. 1979;59:245–258. doi: 10.1007/BF00927519. DOI
Stoitsova SR, Georgiev BB, Dacheva RB. Ultrastructure of spermiogenesis and the mature spermatozoon of Tetrabothrius erostris Loennberg, 1896 (Cestoda, Tetrabothriidae) Int. J. Parasitol. 1995;25:1427–1436. doi: 10.1016/0020-7519(95)00075-5. PubMed DOI
Anderson WA, Personne P. The localization of glycogen in the spermatozoa of various invertebrate and vertebrate species. J. Cell. Biol. 1970;4:29–51. doi: 10.1083/jcb.44.1.29. PubMed DOI PMC
Fawcett DW, Porter KR. A study of the fine structure of ciliated epithelia. J. Morphol. 1954;94:221–82. doi: 10.1002/jmor.1050940202. DOI
Manton, I. & Clarke, B. An electron microscope study of the spermatozoid of sphagnum. J. Exp. Bot. 3, 265–74, https://www.jstor.org/stable/23686102 (1952).
Burton PR, Silveira M. Electron microscopic and optical diffraction studies of negatively stained axial units of certain platyhelminth sperm. J. Ultrastruct. Res. 1971;36:757–767. doi: 10.1016/S0022-5320(71)90029-3. PubMed DOI
Ergens, R. & Lom, J. Causative agents of fish diseases. 384 pp. (Academia 1970).
Mastronarde DN. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005;152:36–51. doi: 10.1016/j.jsb.2005.07.007. PubMed DOI
Mastronarde DN. Dual-axis tomography: an approach with alignment methods that preserve resolution. J. Struct. Biol. 1997;120:343–352. doi: 10.1006/jsbi.1997.3919. PubMed DOI
Crowther RA, Henderson R, Smith JM. MRC Image processing programs. J. Struct. Biol. 1996;116:9–16. doi: 10.1006/jsbi.1996.0003. PubMed DOI