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Licensed Unlicensed Requires Authentication Published by De Gruyter June 16, 2015

Molecular phylogeny and ultrastructure of Myxobolus cf. cuneus, a parasite of patinga hybrid and Henneguya pseudoplatystoma, a parasite of pintado hybrid

Tiago Milanin, Antônio Augusto Mendes Maia, Márcia Ramos Monteiro Silva, Mateus Maldonado Carriero and Edson Aparecido Adriano
From the journal Acta Parasitologica


Through morphological, histopathological and ultrastructural analysis of Myxobolus cuneus Adriano, Arana et Cordeiro, 2006 and Henneguya pseudoplatystoma Naldoni, Arana, Maia, Ceccarelli, Tavares, Borges, Pozo et Adriano, 2009 were identified infecting pacu respectively (Piaractus mesopotamicus) and hybrid pintado (Pseudoplatystoma corruscans x Pseudoplatystoma reticulatum) taken from Brazilian fish farms. The present study describes 18S rDNA sequencing of Myxobolus cf. cuneus infecting the spleen of farmed patinga, a hybrid fish resulting from the crossing of P. mesopotamicus x Piaractus brachypomus, and H. pseudoplatystoma found in farmed hybrid pintado from the state of Sao Paulo, Brazil. The study also provides new details of the host-parasite interface of M. cf. cuneus, which reveal that the plasmodial wall is composed of a single membrane connected to the plasmodium ectoplasm by numerous pinocytic canals. The plasmodia also displayed asynchronous development but had disporic pansporoblasts at different developmental stages; immature and mature spores were found at different depth levels of the plasmodium. Maximum likelihood phylogenetic analysis showed that M. cf. cuneus appeared as a sister species of Henneguya pellucida Adriano, Arana et Cordeiro, 2005 in a sub-clade composed mainly of myxosporean parasites of characiforms, and that H. pseudoplatystoma clustered in a sub-clade composed of Henneguya/Myxobolus spp. parasites of siluriform fish.


Adriano E A., Arana S., Cordeiro N. S. 2005a. An ultrastructural and histopathological study of Henneguya pellucida n.sp. (Myxosporea: Myxobolidae) infecting Piaractus mesopotamicus (Characidae) cultivated in Brazil. Parasite, 12, 221-227. DOI: in Google Scholar

Adriano E.A., Arana S., Cordeiro N.S. 2005b. Histology, ultrastructure and prevalence of Henneguya piaractus (Myxosporea) infecting the gills of Piaractus mesopotamicus (Characidae) cultivated in Brazil. Diseases Aquatic Organisms, 64, 229-35. DOI: in Google Scholar

Adriano E.A., Arana S., Cordeiro, N.S. 2006. Histopathology and ultrastructure of Myxobolus cuneus n. sp. infecting the connective tissue of Piaractus mesopotamicus (Pisces: Characidae) cultivated in Brazil. Parasite, 13, 137-42. DOI: in Google Scholar

Adriano E.A., Carriero M.M., Maia A.A. M., Silva M.R.M., Naldoni J., Ceccarelli S.P., Arana S. 2012. Phylogenetic and host-parasite relationship analysis of Henneguya multiplasmodialis n. sp. Infecting Pseudoplatystoma spp. in Brazilian Pantanal wetland. Veterinary Parasitology, 185, 110−120. DOI: in Google Scholar

Altschul S.F., Madden T.L., Schaffer A.A., Zhang J.H., Zhang Z., Miller W., Lipman D.J. 1997. Gapped BLAST and PSIBLAST: a new generation of protein database search programs. Nucleic Acids Research, 25, 3389−3402. DOI: 10. 1093/nar/25.17.338910.1093/nar/25.17.3389Search in Google Scholar

Barta J.R., Martin D.S., Liberator P.A., Dashkevicz M., Anderson J. W., Feighner S.D., Elbrecht A., Perkins-Barrow A., Jenkins M.C., Danforth H.D., Ru_ M.D., Profous-Juchelka H. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal Parasitology, 83, 262-271. DOI: 10.2307/328445310.2307/3284453Search in Google Scholar

Carriero M.M., Adriano E.A., Silva M.R.M., Ceccarelli P.S., Maia A.A.M. 2013. Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS One, 8, e73713, 1-2. DOI: in Google Scholar

Carvalho D.C., Seerig A., Melo D.C., Sousa A.B., Pimenta D., Oliveira D.A.A. 2008. Identificacao molecular de peixes: o caso do Surubim (Pseudoplatystoma spp.). Revista Brasileira de Reprodução Animal, 32, 215-219Search in Google Scholar

Current W.L., Janovy J.Jr. 1976. Ultrastructure of interlamellar Henneguya exilis in the channel catfish. Journal Parasitology, 62, 975-981. DOI: 10.2307/327919310.2307/3279193Search in Google Scholar

Current W.L., Janovy J.Jr. 1978. Comparative study of ultrastructure of interlamellar and intralamellar types of Henneguya exilis Kudo from channel catfish. Journal of Protozoology, 25, 56-6510.1111/j.1550-7408.1978.tb03868.xSearch in Google Scholar

Current W.L. 1979. Henneguya adiposa Minchew (Myxosporida) in the channel catfish: ultrastructure of the plasmodium wall and sporogenesis. Journal of Protozoology, 26, 209-217. DOI: 10.1111/j.1550-7408.1979.tb02762.x 10.1111/j.1550-7408.1979.tb02762.xSearch in Google Scholar

Diamant A., Whipps C.M., Kent M.L. 2004. A new species of Sphaeromyxa (Myxosporea: Sphaeromyxina: Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern Red Sea: Morphology, ultrastructure, and phylogeny. Journal parasitology, 90, 1434-144210.1645/GE-336RSearch in Google Scholar

Eiras J.C. 2002. Synopsis of the species of the genus Henneguya Thelohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 52, 43-5410.1023/A:1015016312195Search in Google Scholar

Eiras J.C., Molnar K., Lu Y.S. 2005. Synopsis of the species of Myxobolus Butschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 61, 1-46. DOI: 10.1007/s11230-004-6343-910.1007/s11230-004-6343-9Search in Google Scholar

Eiras J.C., Adriano E.A. 2012. A checklist of new species of Henneguya Thelohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012. Systematic Parasitology, 83, 95-104. DOI: 10.1007/s11230-012-9374-710.1007/s11230-012-9374-7Search in Google Scholar

Eiras J.C., Zhang J., Molnar. K. 2014. Synopsis of the species of Myxobolus Butschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Systematic Parasitology 88, 11-36. DOI: 10.1007/s11230-014-9484-510.1007/s11230-014-9484-5Search in Google Scholar

El-Mansy A., Bashtar A.R. 2002. Histopathological and ultrastructural studies of Henneguya suprabranchiae Landsberg, 1987 (Myxosporea: Myxobolidae) parasitizing the suprabranchial organ of the freshwater catfish Clarias gariepinus Burchell, 1822 in Egypt. Parasitology Research, 88, 617-626. DOI: 10.1007/s00436-002-0598-310.1007/s00436-002-0598-3Search in Google Scholar

Eszterbauer E. 2004. Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Diseases Aquatic Organisms, 58, 35-40. DOI: 10.3354/dao05803510.3354/dao058035Search in Google Scholar

FAO (Food and Agriculture Organization of the United Nations). 2012. The state of world fisheries and aquaculture 2012. FAO. Rome. Available in: Accessed at February 04, 2014Search in Google Scholar

Feist S. W., Longshaw M. 2006. Phylum myxozoa. In: PTK Woo (ed.), Fish diseases and disorders. Protozoan and metazoan infections. 2nd ed. CAB International, Oxfordshire. 1:230-29610.1079/9780851990156.0230Search in Google Scholar

Fiala I. 2006. The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal of Parasitology, 36, 1521-1534. DOI: 10.1016/j.ijpara. 2006.06.016Search in Google Scholar

Franceschini L. 2012. Infeccoes parasitarias e microbianas na producao do pacu Piaractus mesopotamicus e do hibrido patinga procedentes da regiao Noroeste do Estado de Sao Paulo. Mastery Degree Thesis, Universidade Estadual Paulista, Institute of Biosciences of Botucatu, Sao Paulo, Brazil Search in Google Scholar

Froese R., Pauly D. 2011. FishBase. World Wide Web electronic publication. Available in: <> Accessed at February 04, 2014Search in Google Scholar

Gomez D., Bartholomew J., Sunyer J. O. 2014. Biology and mucosal immunity to myxozoans. Developmental & Comparative Immunology, 43, 243-256. DOI: 10.1016/j.dci.2013.08.014 10.1016/j.dci.2013.08.014Search in Google Scholar

Guindon S., Dufayard J. F., Lefort V., Anisimova M., Hordijk W., Gascuel O. 2010. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307-321. DOI: 10. 1093/sysbio/syq010.Search in Google Scholar

Hall T. A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95-98.Search in Google Scholar

Hallett S. L., Diamant A. 2001. Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n.sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland, Australia. Diseases Aquatic Organisms, 46, 197-212. DOI: 10.3354/dao046197.10.3354/dao046197Search in Google Scholar

Holzer A. S., Schachner O. 2002. Myxobolus cycloides on the swimbladder of chub Leuciscus cephalus: a controlled, host-specific localization. Diseases Aquatic Organisms, 49, 179-183. DOI: 10.3354/dao04917910.3354/dao049179Search in Google Scholar

IBAMA - Instituto Brasileiro do Meio Ambiente e dos Recursos Naturais Renovaveis. 2008. Estatistica da pesca 2006 Brasil: grandes regioes e unidades da federacao, IBAMA, Brasilia, pp. 181Search in Google Scholar

Martins M.L., Souza V.N., Moraes F.R., Moraes J.R.E., Costa A.J., Rocha U.F. 1997. Pathology and behavioral effects associated with Henneguya sp. (Myxozoa: Myxobolidae) infections of captive pacu Piaractus mesopotamicus in Brazil. Journal World Aquaculture Society, 28, 297-300. DOI: 10.1111/ j.1749-7345.1997.tb00646.x 10.1111/j.1749-7345.1997.tb00646.xSearch in Google Scholar

Milanin T., Eiras J.C., Arana S., Maia A.A.M., Alves A.L., Silva M.R.M., Carriero M.M., Ceccarelli P.S., Adriano E.A. 2010. Phylogeny, Ultrastructure, histopathology and prevalence of Myxobolus oliveirai sp. nov., a parasite of Brycon Hilarii (Characidade) in the Pantanal wetland, Brazil. Memórias Instituto Oswaldo Cruz, 105, 762-769. DOI: 10.1590/S0074-0276201000060000610.1590/S0074-02762010000600006Search in Google Scholar

Molnár K., Eszterbauer E., Szekely C., Dan A., Harrach B. 2002. Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal Fish Diseases, 25, 643-652. DOI: 10.1046/j.1365-2761.2002.00409.x 10.1046/j.1365-2761.2002.00409.xSearch in Google Scholar

MPA. 2011. Boletim estatistico da pesca e aquicultura, Brasil. Brasilia: Ministerio da Pesca e Aquicultura, pp. 60Search in Google Scholar

Muller I.M., Adriano A.E., Ceccarelli S.P., Silva M.R.M., Maia M.A.A., Ueta T.M. 2013: Prevalence, intensity, and phylogenetic analysis of Henneguya piaractus and Myxobolus cf. colossomatis from farmed Piaractus mesopotamicus in Brazil. Diseases Aquatic Organisms, 107, 129-139. DOI: 10.3354/dao0266810.3354/dao02668Search in Google Scholar

Naldoni J., Arana S., Maia A.A.M., Ceccarelli P.S., Tavares L.E.R., Borges F. A., Pozo C. F., Adriano E. A. 2009. Henneguya pseudoplatystoma n. sp. causing reduction in epithelial area of gills in the farmed pintado, a South American catfish: Histopathology and ultrastructure. Veterinary Parasitology, 166, 52-59. DOI: 10.1016/j.vetpar.2009.07.03410.1016/j.vetpar.2009.07.034Search in Google Scholar

Naldoni J., Arana S., Maia A.A.M., Silva M.R.M., Carriero M.M., Ceccarelli P.S., Tavares L.E.R., Adriano, E.A. 2011. Host-parasite- environment relationship, morphology and molecular analyses of Henneguya eirasi n. sp. parasite of two wild Pseudoplatystoma spp. in Pantanal Wetland, Brazil. Veterinary Parasitology, 177, 247-255. DOI: 10.1016/j.vetpar. 2010.12.008Search in Google Scholar

Naldoni J., Maia A.A.M., Silva M.R.M., Adriano E.A. 2014. Henneguya cuniculator sp. nov., a parasite of spotted sorumbim Pseudoplatystoma corruscans in the Sao Francisco Basin, Brasil. Diseases Aquatic Organisms, 107, 211-22110.3354/dao02685Search in Google Scholar

Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253-1256. DOI: 10.1093/ molbev/msn08310.1093/molbev/msn083Search in Google Scholar

Rocha E., Matos E., Azevedo C. 1992. Henneguya amazônica n. sp. (Myxozoa, Myxobolidae), parasitizing the gills of Crenicichla lepidota Heckel, 1840 (Teleostei, Cichlidae) from the Amazon river. European Journal of Protistology, 28, 273-27810.1016/S0932-4739(11)80233-6Search in Google Scholar

Sitjà-Bobadilla A. 2008. Fish immune response to myxozoan parasites. Parasite, 15, 420-42510.1051/parasite/2008153420Search in Google Scholar

Sitjà-Bobadilla A., Alvarez-Pellitero P. 1993. Pathologic effects of Sphaerospora dicentrarchi Sitj/t-Bobadilla and Alvarez-Pellitero, 1992 and S. testicularis Sitja-Bobadilla and Alvarez- Pellitero, 1990 (Myxosporea: Bivalvulida) parasitic in the Mediterranean sea bass Dicentrarchus labrax L. (Teleostei: Serranidae) and the cell-mediated immune reaction: a light and electron microscopy study. Parasitology Research, 79, 119-129. DOI: 10.1007/BF0093225710.1007/BF00932257Search in Google Scholar

Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28, 2731-2739. DOI: 10.1093/molbev/msr12110.1093/molbev/msr121Search in Google Scholar

Urbinati E.C., Goncalves F.D., Takahashi L.S. 2010. Pacu (Piaractus mesopotamicus). In: Baldisserotto B. and Gomes L.C. Especies nativas para piscicultura no Brasil. UFSM, Santa Maria, p. 205-244 Search in Google Scholar

Received: 2014-10-14
Revised: 2015-1-23
Accepted: 2015-3-13
Published Online: 2015-6-16
Published in Print: 2015-9-1

© W. Stefański Institute of Parasitology, PAS