Abstract
In the course of experimental infections of gilthead sea bream Sparus aurata with the myxozoan Enteromyxum leei, stages of an unidentified myxozoan were observed attached to the intestinal brush border of some fish. Infection levels of the parasite, which was named “epi-epithelial myxosporean” (EEM) were recorded, and its structure was studied by light microscopy (LM) and electron microscopy (EM). In situ hybridisation (ISH) probes specific for E. leei were developed and used to differentiate between the two parasites. The EEM parasite was observed only in epi-epithelial position on the intestine mucosa and never in any of the other tissues studied (kidney and gall bladder). Prevalence was variable, with values reaching 40.2%. With transmission EM, trophozoites displayed pseudopodia-like projections inserted in between the enterocyte microvilli, producing an intimate interface. No mucosal histopathology that could be attributed to the myxozoan was found. EEM stages did not stain with the E. leei-specific ISH probes. From the results of the LM, EM and ISH studies, we conclude that the EEM parasite found in gilthead sea bream intestine in both Mediterranean and Red Sea sites is a coelozoic myxosporean, distinct from E. leei.
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References
Àlvarez-Pellitero P, Sitjà-Bobadilla A (1993) Pathology of Myxosporea in marine fish culture. Dis Aquat Org 17:229–238
APROMAR (2006) La acuicultura marina de peces en España. Available online at http://www.apromar.es/informes.asp
Athanassopoulou F, Karagouni E, Dotsika E, Ragias V, Tavla J, Christofilloyanis P (2004) Efficacy and toxicity of orally administered anticoccidial drugs for innovative treatments of Polysporoplasma sparis (Sitjà-Bobadilla and Álvarez-Pellitero 1985) infection in Sparus aurata L. J Appl Ichthyol 20:345–354
Canning EU, Okamura B (2004) Biodiversity and evolution of Myxozoa. Adv Parasitol 56:43–131
Canning EU, Curry A, Anderson CL, Okamura B (1999) Ultrastructure of Myxidium trachinorum sp. nov. from the gallbladder of the lesser weever fish Echiichtys vipera. Parasitol Res 85:910–919
Cho JB, Kwon SR, Kim SK, Nam YK, Kim KH (2004) Ultrastructure and development of Ceratomyxa protopsettae fujita, 1923 (Myxosporea) in the gallbladder of cultured olive flounder, Paralichthys olivaceus. Acta Protozool 43:241–250
Diamant A (1997) Fish-to-fish transmission of a marine myxosporean. Dis Aquat Org 30:99–105
Diamant A, Paperna I (1992) Zschokkella icterica sp. nov. (Myxozoa, Myxosporea), a pathogen of wild rabbit fish Siganus luridus (Ruppell, 1829) from the Red Sea. Eur J Protistol 28:71–78
Diamant A, Whipps CM, Kent ML (2004) Sphaeromyxa zaharoni n. sp. (Myxosporea: Sphaeromyxina: Sphaeromyxidae), a parasite of devil firefish Pterois miles (Scorpaenidae) from the northern Red Sea: morphology, ultrastructure and phylogeny. J Parasitol 90(6):1434–1442
El-Matbouli M, Hoffmann RW (1994) Sinuolinea tetraodoni n. sp., a myxosporean parasite of freshwater pufferfish Tetraodon palembangensis from Southeast Asia- light and electron microscope observations. Dis Aquat Org 19:47–54
Golomazou E, Karagouni E, Athanassopoulou F (2004) The most important myxosporean parasite species affecting cultured Mediterranean fish. J Hell Vet Med Soc 55:342–352
Hulbert WC, Komourdijan MP, Moon TW, Fenwick JC (1977) The fine structure of sporogony in Myxidium zealandicum (Protozoa: Myxosporidia). Can J Zool 55:438–447
Kent ML, Andrée KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallet SL, Lester RJG, Longshaw M, Palenzuela O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413
Lom J, Dyková I (1992) Protozoan parasites of fishes. Developments in aquaculture and fisheries science, vol 26. Elsevier, Amsterdam
Lom J, Dyková (2006) Myxozoa genera: definition and notes on taxonomy, life cycle terminology and pathogenic species. Folia Parasitol 53:1–36
Morrison CM, Martell DJ, Leggiadro C, Oneil D (1996) Ceratomyxa drepanosepttae in the gallbladder of Atlantic halibut, Hipoglossus hipoglossus, from the North West Atlantic Ocean. Folia Parasitol 43:20–36
Palenzuela O (2006) Myxozoan infections in Mediterranean mariculture. Parassitologia 48:27–29
Palenzuela O, Bartholomew JL (2002) Molecular tools for the diagnosis of Ceratomyxa shasta (Myxozoa). In: Cunningham CO (ed) Molecular diagnosis of salmonid diseases. Kluwer, The Netherlands, pp 285–298
Palenzuela O, Sitjà-Bobadilla A, Álvarez-Pellitero P (1997) Ceratomyxa sparusaurati (Protozoa: Myxosporea) infections in cultured gilthead seabream Sparus aurata (Pisces:Teleostei) from Spain: aspects of the host-parasite relationship. Parasitol Res 83:539–548
Palenzuela O, Álvarez-Pellitero P, Sitjà-Bobadilla A (1999) Glomerular disease associated to Polysporoplasma sparis (Myxosporea: Bivalvulida) infections in the gilthead sea bream, Sparus aurata, (Pisces; Teleostei): aspects of the host–parasite relationship. Parasitology 118:245–256
Palenzuela O, Redondo MJ, Álvarez-Pellitero P (2002) Description of Enteromyxum scophthalmi gen nov., sp. nov. (Myxozoa), an intestinal parasite of turbot (Scophthalmus maximus L.) using morphological and ribosomal RNA sequence data. Parasitology 124:369–379
Sitjà-Bobadilla A (2004) Parasites in Mediterranean aquacultured fish: current impact and future research directions. In: Mas-Coma S (ed) Multidisciplinarity for parasites, vectors and parasitic diseases. Medimond, Bologna, Italy, pp 301–311
Sitjà-Bobadilla A, Álvarez-Pellitero P (1993) Zschokkella mugilis n.sp. (Myxosporea, Bivalvulida) from mullets (Teleostei, Mugilidae) of Mediterranean waters—light and electron microscopic description. J Eukaryot Microbiol 40:755–764
Sitjà-Bobadilla A, Álvarez-Pellitero P (2001) Leptotheca sparidarum N. Sp. (Myxosporea: Bivalvulida), a parasite from cultured common dentex (Dentex dentex L.) and gilthead sea bream (Sparus aurata L.) (Teleostei: Sparidae). J Eukaryot Microbiol 48:627–639
Sitjà-Bobadilla A, Diamant A, Palenzuela O, Álvarez-Pellitero P (2007) Host factors and experimental conditions on the horizontal transmission of Enteromyxym leei (Myxozoa) to gilthead sea bream (Sparus aurata L.) and European sea bass (Dicentrarchus labrax L.). J Fish Dis 29:1–8
Su XQ (1996) An ultrastructural study of Zschokkella leptatherinae (Myxozoa: Myxosporea) from atherinid fish, Leptatherina presbyteroides. Acta Protozool 35:41–48
Tin Tun, Yokoyama H, Ogawa K, Wakabayashi H (2000) Myxosporeans and their hyperparasitic microsporeans in the intestine of emaciated tiger puffer. Fish Pathol 35:145–156
Upenskaya AV (1982) New data on the life cycle and biology of Myxosporidia. Arch Protistenkd 126:309–338
Yanagida T, Nomura Y, Kimura T, Fukuda Y, Yokoyama H, Ogawa K (2004) Molecular and morphological redescriptions of enteric Myxozoans, Enteromyxum leei (formerly Myxidium sp. TP) and Enteromyxum fugu comb. N. (syn. Myxidium fugu) from cultured tiger puffer. Fish Pathol 39:137–143
Yanagida T, Sameshima M, Nasu H, Yokoyama H, Ogawa K (2006) Temperature effects on the development of Enteromyxum spp (Myxozoa) in experimentally infected tiger puffer, Takifugu rubripes (Temmink & Schlegel). J Fish Dis 29:561–567
Yasuda H, Ooyama T, Izawa K, Tun T, Yokoyama H, Ogawa K (2002) Fish-to-fish transmission of Myxidium spp. (Myxozoa) in cultured tiger puffer suffering from emaciation disease. Fish Pathol 37:29–33
Acknowledgement
The authors would like to thank Mr. Lluis Puig for his contribution to this work. We also acknowledge excellent technical support from the transmission electron microscopy service of UAB. The authors declare that the experimental procedures performed for this work comply with current laws of Spain and Israel.
Funding for this work was obtained from the European Union through research project QLRT-2001-00722 (MyxFishControl). M. Cuadrado benefits from a FI grant from “Departament d’Universitats, Recerca i Societat de la Informació” of the Generalitat de Catalunya and the European Social Fund.
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Cuadrado, M., Albinyana, G., Padrós, F. et al. An unidentified epi-epithelial myxosporean in the intestine of gilthead sea bream Sparus aurata L.. Parasitol Res 101, 403–411 (2007). https://doi.org/10.1007/s00436-007-0484-0
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DOI: https://doi.org/10.1007/s00436-007-0484-0