Architecture of Paradiplozoon homoion: A diplozoid monogenean exhibiting highly-developed equipment for ectoparasitism

. 2018 ; 13 (2) : e0192285. [epub] 20180207

Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid29414983

Diplozoidae (Monogenea) are blood-feeding freshwater fish gill ectoparasites with extraordinary body architecture and a unique sexual behaviour in which two larval worms fuse and transform into one functioning individual. In this study, we describe the body organisation of Paradiplozoon homoion adult stage using a combined approach of confocal laser scanning and electron microscopy, with emphasis on the forebody and hindbody. Special attention is given to structures involved in functional adaptation to ectoparasitism, i.e. host searching, attachment and feeding/metabolism. Our observations indicate clear adaptations for blood sucking, with a well-innervated mouth opening surrounded by sensory structures, prominent muscular buccal suckers and a pharynx. The buccal cavity surface is covered with numerous tegumentary digitations that increase the area in contact with host tissue and, subsequently, with its blood. The buccal suckers and the well-innervated haptor (with sclerotised clamps controlled by noticeable musculature) cooperate in attaching to and moving over the host. Putative gland cells accumulate in the region of apical circular structures, pharynx area and in the haptor middle region. Paired club-shaped sacs lying laterally to the pharynx might serve as secretory reservoirs. Furthermore, we were able to visualise the body wall musculature, including peripheral innervation, the distribution of uniciliated sensory structures essential for reception of external environmental information, and flame cells involved in excretion. Our results confirm in detail that P. homoion displays a range of sophisticated adaptations to an ectoparasitic life style, characteristic for diplozoid monogeneans.

Zobrazit více v PubMed

Poulin R. Evolutionary ecology of parasites: from individuals to communities. London: Chapman and Hall; 1998.

Smyth JD, Halton DV. The physiology of trematodes. Cambridge: Cambridge University Press; 1983.

Nordmann A. Mikrographische Beiträge zur Naturgeschichte der wirbellosen Thiere. Academie Berlin. 1832; 2:57–76. German.

Zeller E. Untersuchungen über die Entwicklung von Diplozoon paradoxum. Z Wiss Zool. 1872; 22:168–180. German.

Goto S. On Diplozoon nipponicum n. sp. J Coll Sci Imp Univ Tokio. 1891; 4:151–192.

Bovet J. Contribution à la morphologie et à la biologie de Diplozoon paradoxum von Nordmann, 1832. Bull. Soc. Neuchâtel. Sci. Nat. 1967; 90:63–159. French.

Khotenovsky IA. Fauna of the USSR. Monogenea Suborder Octomacrinae Khotenovsky. Leningrad: Nauka; 1985. Russian.

Halton DW. Microscopy and the helminth parasite. Micron. 2004;35:361–390. doi: 10.1016/j.micron.2003.12.001 PubMed DOI

Buchmann K, Lindenstrøm T. Interactions between monogenean parasites and their fish hosts. Int. J Parasitol. 2002; 32:309–319. PubMed

Sterba G. Zur Morfologie und Biologie der Gattung Diplozoon (Untersuchungen an Diplozoon tetragonopterini spec. nov.). Zool Anz. 1957; 158:181–196. German.

Kamegai S, Ichigara A, Kato K, Nonobe H, Machida M. Diplozoon nipponicum Goto, 1891. Part I: Morfological observation on the worms obtained from Cyprinus carpio. Month Rep Meguro Parasitol Mus. 1966; 83–84:1–9. Japanese.

Hirose H, Akamatsu H, Hibiya T. On the development of clamps and pairing of dipropae in Diplozoon nipponicum (Monogeenea). Bull Japan Soc Sci Fish. 1987; 53(6):953–957.

Schabussova I, Schabuss M, Gelnar M, Horák P. Use of lectins in characterizing developmentally regulated changes on the surface of Paradiplozoon megan (Monogenea: Diplozoidae). Helminthologia. 2003; 40:135–140.

Zurawski TH, Mousley A, Maule AG, Gelnar M, Halton DW. Cytochemical studies of the neuromuscular systems of the diporpa and juvenile stages of Eudiplozoon nipponicum (Monogenea: Diplozoidae). Parasitology. 2003; 126:349–357. PubMed

Schabussova I, Koubkova B, Gelnar M, Schabuss M, Horák P. Surface carbohydrates of Eudiplozoon nipponicum pre- and post-fusion. J Helminthol. 2004; 78:63–68. PubMed

Hodová I, Matejusova I, Gelnar M. The surface topography of Eudiplozoon nipponicum (Monogenea) developmental stages parasitizing carp (Cyprinus carpio L.). Cent Eur J Biol. 2010; 5(5):702–709.

Valigurová A, Hodová I, Sonnek R, Koubková B, Gelnar M. Eudiplozoon nipponicum in focus: monogenean exhibiting a highly specialized adaptation for ectoparasitic lifestyle. Parasitol Res. 2011; 108(2): 383–394. doi: 10.1007/s00436-010-2077-6 PubMed DOI

Matejusová I, Koubková B, D´Amelio SD, Cunningham CO. Genetic characterization of six species of diplozoids (Monogenea; Diplozoidae). Parasitology. 2001; 123:465–474. PubMed

Matejusová I, Koubková B, Gelnar M, Cunningham CO. Paradiplozoon homoion Bychowsky & Nagibina, 1959 versus P. gracile Reichenbach-Klinke, 1961 (Monogenea): two species or phenotypic plasticity? Syst Parasitol. 2002; 53:39–47. PubMed

Matejusová I, Koubková B, Cunningham CO. Identification of European diplozoids (Monogenea, Diplozoinae) by restriction digestion of the ribosomal RNA internal transcribed spacer. J Parasitol. 2004; 90(4):817–822. doi: 10.1645/GE-138R PubMed DOI

Košková E, Matějusová I, Civáňová K, Koubková B. Ethanol-fixed material used for both classical and molecular identification purposes: Eudiplozoon nipponicum (Monogenea: Diplozoidae) as a case parasite species. Parasitol Res. 2010; 107:909–914. doi: 10.1007/s00436-010-1949-0 PubMed DOI

Civáňová K, Koyun M, Koubková B. The molecular and morphometrical description of a new diplozoid species from the gills of the Garra rufa (Heckel, 1843) (Cyprinidae) from Turkey–including a commentary on taxonomic division of Diplozoidae. Parasitol Res. 2013; 112:3053–3062. doi: 10.1007/s00436-013-3480-6 PubMed DOI

Košková E, Špakulová M, Koubková B, Reblánová M, Orosová M. Comparative karyological analysis of four diplozoid species (Monogenea, Diplozoidae), gill parasites of cyprinid fishes. Parasitol Res. 2011; 108:935–941. doi: 10.1007/s00436-010-2135-0 PubMed DOI

Bombarová M, Špakulová M, Koubková B. New data on the karyotype and chromosomal rDNA location in Paradiplozoon megan (Monogenea, Diplozoidae), gill parasite of chubs Parasitol Res. 2014; 113:4111–4116. doi: 10.1007/s00436-014-4082-7 PubMed DOI

Zurawski TH, Mousley A, Mair GR, Brennan GP, Maule AG, Gelnar M, et al. Immunomicroscopical observations on the nervous system of adult Eudiplozoon nipponicum (Monogenea: Diplozoidae). Int J Parasitol. 2001; 31(8):783–792. PubMed

Zurawski TH, Mair GR, Maule AG, Gelnar M, Halton DW. Microscopical evaluation of neural connectivity between paired stages of Eudiplozoon nipponicum (Monogenea: Diplozoidae). J. Parasitol. 2003; 89(1):198–200. doi: 10.1645/0022-3395(2003)089[0198:MEONCB]2.0.CO;2 PubMed DOI

Jedličková L, Dvořáková H, Kašný M, Ilgová J, Potěšil D, Zdráhal Z, et al. Major acid endopeptidases of the blood-feeding monogenean Eudiplozoon nipponicum (Heteronchoinea: Diplozoidae). Parasitology. 2016; 143:494–506. doi: 10.1017/S0031182015001808 PubMed DOI

Ilgová J, Jedličková L, Dvořáková H, Benovics M, Mikeš L, Janda L, et al. A novel type I cystatin of parasite origin with atypical legumain-binding domain. Sci Rep. 2017; 7:17526 doi: 10.1038/s41598-017-17598-2 PubMed DOI PMC

Pečínková M, Matějusová I, Koubková B, Gelnar M. Investigation of Paradiplozoon homoion (Monogenea, Diplozoidae) life cycle under experimental conditions. Parasitol Int. 2007; 56:179–183. doi: 10.1016/j.parint.2007.01.010 PubMed DOI

Pečínková M, Matějusová I, Koubková B, Gelnar M. Classification and occurrence of abnormally developed Paradiplozoon homoion (Monogenea, Diplozoinae) parasitising gudgeon Gobio gobio. Dis Aquat Organ. 2005; 64:63–68. doi: 10.3354/dao064063 PubMed DOI

Pečínková M, Vøllestad LA, Koubková B, Gelnar M. Asymmetries in the attachment apparatus of a gill parasite. J Zool. 2007; 272:406–414.

Pečínková M, Vøllestad LA, Koubková B, Huml J, Jurajda P, Gelnar M. The relationship between developmental instability of gudgeon Gobio gobio and abundance or morphology of its ectoparasite Paradiplozoon homoion (Monogenea). J Fish Biol. 2007; 71:1358–1370.

Konstanzová V, Koubková B, Kašný M, Ilgová J, Dzika E, Gelnar M. Ultrastructure of the digestive tract of Paradiplozoon homoion (Monogenea). Parasitol Res. 2015; 114:1485–1494. doi: 10.1007/s00436-015-4331-4 PubMed DOI

Konstanzová V, Koubková B, Kašný M, Ilgová J, Dzika E, Gelnar M. Excretory system of representatives from family Diplozoidae (Monogenea). Parasitol Res. 2016; 115:1493–1500. doi: 10.1007/s00436-015-4882-4 PubMed DOI

Konstanzová V, Kašný M, Ilgová J, Dzika E, Gelnar M. An ultrastructural study of the surface and attachment structures of Paradiplozoon homoion (Bychowsky & Nagibina, 1959) (Monogenea: Diplozoidae). Parasite Vector. 2017; 10:261. PubMed PMC

Milne SJ, Avenant-Oldewage A. The fluorescent detection of Paradiplozoon sp. (Monogenea: Diplozoidae) attachment clamps‘ sclerites and integumental proteins. Onderstepoort J Vet Res. 2006; 73:149–152. PubMed

Avenant-Oldewage A, Milne SJ. Aspects of the morphology of the juvenile life stages of Paradiplozoon ichthyoxanthon Avenant-Oldewage, 2013 (Monogenea: Diplozoidae). Acta Parasitol. 2014; 59(2):247–254. doi: 10.2478/s11686-014-0235-1 PubMed DOI

Dos Santos QM, Avenant-Oldewage A. Soft tissue digestion of Paradiplozoon vaalense for SEM of sclerites and simultaneous molecular analysis. J Parasitol. 2015; 101(1):94–97. doi: 10.1645/14-521.1 PubMed DOI

Gilbert BM, Avenant-Oldewage A. Trace element and metal sequestration in vitellaria and sclerites, and reactive oxygen intermediates in a freshwater monogenean, Paradiplozoon ichthyoxanthon. PLoS One. 2017; 12(5):e0177558 doi: 10.1371/journal.pone.0177558 PubMed DOI PMC

Collins JJ III, King RS, Cogswell A, Williams DL, Newmark PA. An atlas for Schistosoma mansoni organs and life-cycle stages using cell type-specific markers and confocal microscopy. PLoS Negl Trop Dis. 2011; 5(3):e1009 doi: 10.1371/journal.pntd.0001009 PubMed DOI PMC

Ergens R, Lom J. Causative agents of fish diseases. Prague: Publishing House Academia; 1970. Czech.

Galli P, Strona G, Villa AM, Benzoni F, Stefani F, Doglia SM, et al. Three-dimensional imaging of monogenoidean sclerites by laser scanning confocal fluorescence microscopy. J Parasitol. 2006; 92(2):395–399. doi: 10.1645/GE-3544RN.1 PubMed DOI

Neves RH, de Lamare Biolcini C, Machado-Silva JR, Carvalho JJ, Branquinho TB, Lenzi HL, et al. A new description of the reproductive system of Schistosoma mansoni (Trematoda: Schistosomatidae) analyzed by confocal laser scanning microscopy. Parasitol Res. 2005; 95:43–49. doi: 10.1007/s00436-004-1241-2 PubMed DOI

Wilson RA, Webster LA. Protonephridia. Biol Rev. 1974; 49:127–160. PubMed

Valverde-Islas LE, Arrangoiz E, Vega E, Robert L, Villanueva R, Reynoso-Ducoing O, et al. Visualization and 3d reconstruction of flame cells of Taenia solium Cestoda). PLoS One. 2011; 6(3):e14754 doi: 10.1371/journal.pone.0014754 PubMed DOI PMC

Ramasamy P, Brennan GP, Halton DW. Ultrastructure of the surface structures of Allodiscocotyla diacanthi (Polyopisthocotylea: Monogenea) from the gills of the marine teleost fish, Scomberoides tol. Int J Parasitol. 1995; 25(1):43–54. PubMed

Ramasamy P, Brennan GP. Ultrastructure of the surface structures and haptor of Empleurosoma pyriforme (Ancyrocephalinae; Monopisthocotylea: Monogenea) from the gills of the teleost fish Therapon jarbua. Parasitol Res. 2000; 86:129–139. PubMed

Cohen SC, Kohn A, Baptista-Farias MFD. Scanning and transmission electron microscopy of the tegument of Paranaella luquei Kohn, Baptista-Farias & Cohen, 2000 (Microcotylidae, Monogenea), parasite of a Brazilian catfish, Hypostomus regani. Mem I Oswaldo Cruz. 2001; 96(4):555–560. PubMed

Arafa SZ, El-Naggar MM, Kearn GC. Scanning electron microscope observations on the monogenean skin parasite Macrogyrodactylus congolensis (Prudhoe, 1957) Yamaguti, 1963. Acta Parasitol. 2003; 48(3):163–171.

Halton DW. The surface topography of a monogenean, Diclidophora merlangi revealed by scanning electron microscopy. Z Parasitenkd. 1979; 61:1–12. PubMed

Lyons KM. Sense organs of monogenean skin parasites ending in a typical cilium. Parasitology. 1969; 59:611–623.

Lane NJ, Flores V. Actin filaments are associated with the septate junctions of Invertebrates, Tissue Cell. 1988; 20(2):211–217. PubMed

Cooper GM. The cell: A molecular approach. 2nd ed. Sinauer Associates; 2000.

Duobinis-Gray LF, Toole JE, Corkum KC. Distribution and fine structure of tegumental receptors in Onchocleidus cyanellus (Monogenea: Ancyrocephalinae). Proc Helm Soc Wash. 1985; 52(2):175–179.

Ramasamy P, Hanna REB, Threadgold LT. Scanning and transmission electron microscopic studies of the surface of Vallisia indica (Monogenea, Polyopisthocotylea). Int J Parasitol. 1987; 17(6):1187–1195.

El-Naggar MM, Khidr AA, Kearn GC. Ultrastructural observations on the tegument and associated structures of the monogenean Cichlidogyrus halli typicus (Price & Kirk, 1967) Paperna, 1979. Int J Parasitol. 1991; 21(6):707–713. PubMed

Halton DW, Maule AG, Mair GR, Shaw C. Monogenean neuromusculature: some structural and functional correlates. Int J Parasitol. 1998; 28:1609–1623. PubMed

Mair GR, Maule AG, Shaw C, Halton DW. Muscling in on parasitic flatworms. Parasitol Today. 1998; 14(2):73–76. PubMed

Poddubnaya LG, Xylander WER, Gibson DI. Ultrastructural characteristics of the protonephridial terminal organ and associated ducts of adult specimens of the Aspidogastrea, Digenea and Monogenea, with comments on the relationships between these groups. Syst Parasitol. 2012; 82:89–104. doi: 10.1007/s11230-012-9359-6 PubMed DOI

Lyons KM. The epidermis and sense organs of the Monogenea and some related groups. Adv Parasit. 1973; 11:193–232. PubMed

Kearn GC. Parasitism and the Platyhelminths. London: Chapman and Hall; 1998.

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Eudiplozoon nipponicum: morphofunctional adaptations of diplozoid monogeneans for confronting their host

. 2021 Aug 17 ; 6 (1) : 23. [epub] 20210817

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...