Folia Parasitologica, vol. 62 (2015)

Folia Parasitologica 62:014 (2015) | 10.14411/fp.2015.014

Host-parasite and phylogenetic relationships of Myxobolus filamentum sp. n. (Myxozoa: Myxosporea), a parasite of Brycon orthotaenia (Characiformes: Bryconidae) in Brazil

Juliana Naldoni1, Suellen A. Zatti1, Kassia R.H. Capodifoglio2, Tiago Milanin1, Antônio A.M. Maia2, Marcia R.M. Silva2, Edson A. Adriano1,3
1 Animal Biology Department, Institute of Biology, University of Campinas, São Paulo, Brazil;
2 Veterinary Medicine Department, College of Animal Science and Food Engineering, São Paulo University, São Paulo, Brazil;
3 Biology Science Department, Federal University of São Paulo, São Paulo, Brazil

Myxobolus filamentum sp. n. was found infecting gill filaments of three of 39 Brycon orthotaenia Günther specimens examined (8%), which were taken from the river São Francisco in Minas Gerais state, Brazil. Plasmodia of the parasite were white and long, measuring 5 mm in lenght. Mature spores of M. filamentum sp. n. were oval from the frontal view and biconvex from the lateral view, measuring 7.5-9.7 µm (9.0 ± 0.3 µm) in length and 5.2-7.3 µm (6.2 ± 0.4 µm) in width. The polar capsules were elongated and equal in size, measuring 3.8-5.5 µm (4.7 ± 0.3 µm) in length and 1.3-2.2 µm (1.7 ± 0.1 µm) in width. The development of the parasite led to compression of the adjacent tissues and inflammatory infiltrate with granulocytic cells. Ultrastructural observation revealed that the plasmodia were delimited by two membranes, which had numerous and extensive pinocytotic channels extending into the wide ectoplasm zone. The plasmodial wall exhibited abundant villi-like projections and a thin layer of granular material prevented direct contact between the plasmodial wall and the host tissue. Phylogenetic analysis, based on 18S rDNA, showed M. filamentum sp. n. as a sister species of Myxobolus oliveirai Milanin, Eiras, Arana, Maia, Alves, Silva, Carriero, Ceccarelli et Adriano, 2010, a parasite of other fish species of the genus Brycon Müller et Troschel from South America.

Keywords: taxonomy, 18S rRNA, ultrastructure, granulocytic cells, freshwater fish, Neotropical Region

Received: May 23, 2014; Accepted: October 13, 2014; Published online: February 9, 2015


References

  1. Adriano E.A., Arana S., Carriero M.M., Naldoni J., Ceccarelli P.S., Maia A.A. 2009: Light, electron microscopy and histopathology of Myxobolus salminus n. sp., a parasite of Salminus brasiliensis from the Brazilian Pantanal. Vet. Parasitol. 165: 25-29. Go to original source... Go to PubMed...
  2. Adriano E.A., Arana S., Cordeiro N.S. 2006: Myxobolus cuneus n. sp. (Myxosporea) infecting the connective tissue of Piaractus mesopotamicus (Pisces: Characidae) in Brazil: histopathology and ultrastructural. Parasite 13: 137-142. Go to original source... Go to PubMed...
  3. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. 1997: Gapped BLASTn and PSI-BLAST: a new generation of protein database search programs. Nucl. Acids Res. 25: 3389-3402. Go to original source... Go to PubMed...
  4. Azevedo C., Casal G., Matos P., Alves A., Matos E. 2011: Henneguya torpedo sp. nov. (Myxozoa), a parasite from the nervous system of the Amazonian teleost Brachyhypopomus pinnicaudatus (Hypopomidae). Dis. Aquat. Org. 93: 235-242. Go to original source... Go to PubMed...
  5. Azevedo C., Marques D.K.S., Casal G., Amaral C.M.C., Silva E.V., Matos P., Matos E. 2010: Ultrastructural re-description of Henneguya piaractus (Myxozoa), a parasite of the freshwater fish Piaractus mesopotamicus (Teleostei, Characidae) from the Paraguai River, Brazil. Acta Protozool. 49: 115-120.
  6. Barta J.R., Martin D.S., Liberator P.A., Dashkevicz M., Anderson J.W., Feighner S.D., Elbrecht A., Perkinsbarrow A., Jenkins M.C., Danforth H.D., Ruff M.D.,Profousjuchelka H. 1997: Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J. Parasitol. 83: 262-271. Go to original source... Go to PubMed...
  7. Bartholomew J.L., Atkinson S.D., Hallett S.L., Lowenstine L.J., Garner M.M., Gardiner C.H.; Keel M.K.; Brown J.D. 2008: Myxozoan parasitism in waterfowl. Int. J. Parasitol. 38: 1199-1120. Go to original source... Go to PubMed...
  8. Bonetto A.A., Pignalbergi C. 1965: Myxobolus paranensis (Protozoa, Myxosporidea) una nueva especie parasita del "Dorado" (Saminus maxillosus). Physis 69: 23-26.
  9. Carriero M.M., Adriano E.A., Silva M.R.M., Ceccarelli P.A., Maia A.A.M. 2013: Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS ONE 8: e73713. Go to original source... Go to PubMed...
  10. Casal G., Matos E., Azevedo C. 1997: Some ultrastructural aspects of Henneguya striolata sp. nov. (Myxozoa: Myxosporea), a parasite of the Amazonian fish Serrasalmus striolatus. Parasitol. Res. 83: 93-95. Go to original source... Go to PubMed...
  11. Casal G., Matos E., Azevedo C. 2002: Ultrastructural data on the spore of Myxobolus maculatus n. sp. (phylum Myxozoa), parasite from the Amazonian fish Metynnis maculatus (Teleostei). Dis. Aquat. Org. 51: 107-112. Go to original source... Go to PubMed...
  12. Casal G., Matos E., Azevedo C. 2006: A new myxozoan parasite from the Amazonian fish Metynnis argenteus (Teleostei, Characidae): light and electron microscope observations. J. Parasitol. 92: 817-821. Go to original source... Go to PubMed...
  13. Current W.L., Janovy J. Jr., Knight S.A. 1979: Myxosoma funduli Kudo (Myxosporida) in Fundulus kansae: ultrastructure of the plasmodium wall and of sporogenesis. J. Protozool. 26: 574-583. Go to original source... Go to PubMed...
  14. 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. J. Parasitol. 90: 1434-1442. Go to original source... Go to PubMed...
  15. Eiras J.C., Molnár K., Lu Y.S. 2005: Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst. Parasitol. 61: 1-46. Go to original source... Go to PubMed...
  16. Eiras J.C., Zhang J., Molnár K. 2014: Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae) described between 2005 and 2013. Syst. Parasitol. 88: 11-36. Go to original source... Go to PubMed...
  17. Froese R., Pauly D. (Eds.) 2013: FishBase. World Wide Web electronic publication, www.fishbase.org, 07/2014.
  18. Godinho H.P., Godinho A.L. 1994: Fish communities in southeastern Brazilian river basins submitted to hydroelectric impoundments. Acta. Limnol. Bras. 5: 187-197.
  19. 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. Syst. Biol. 59: 307-321. Go to original source... Go to PubMed...
  20. Hall T.A. 1999: BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucl. Acids Symp. Ser. 41: 95-98. Go to PubMed...
  21. 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. Dis. Aquat. Org. 46: 197-212. Go to original source... Go to PubMed...
  22. Lovy J., Goodwin A.E., Speare D.J., Wadowska D.W., Wright G.M. 2011: Histochemical and ultrastructural analysis of pathology and cell responses in gills of channel catfish affected with proliferative gill disease. Dis. Aquat. Org. 94: 125-134. Go to original source... Go to PubMed...
  23. 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 (Characidae) in the Pantanal wetland, Brazil. Mem. Inst. Oswaldo Cruz 105: 762-769. Go to original source... Go to PubMed...
  24. Molnár K., Ranzani-Paiva M.J., Eiras J.C., Rodrigues E.L. 1998: Myxobolus macroplasmodialis sp. n. (Myxozoa: Myxosporea), a parasite of the abdominal cavity of the characid teleost, Salminus maxillosus, in Brazil. Acta Protozool. 37: 241-245.
  25. Molnár K., Eszterbauer E., Székely C., Dán A., Harrach B. 2002: Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J. Fish Dis. 25: 643-652. Go to original source...
  26. Moreira G.S.A., Adriano E.A., Silva M.R.M., Ceccarelli P.S., Maia A.A.M. 2014: The morphological and molecular characterization of Henneguya rotunda n. sp., a parasite of the gill arch and fins of Salminus brasiliensis from the Mogi Guaçu River, Brazil. Parasitol. Res. 113: 1703-1711. Go to original source... Go to PubMed...
  27. MPA 2012: Ministry of Fisheries and Agriculture (Ministério da Pesca e Aqüicultura): Sporting freshwater fishes (Peixes esportivos de água doce). World Wide Web electronic publication, http://www.mpa.gov.br/index.php/topicos/33-amadora/1285-peixe-matrinxã, 1/2014.
  28. Naldoni J., Maia A.A.M., Silva M.R.M., Adriano E. 2014. Henneguya cuniculator sp. nov., a parasite of spotted sorubim Pseudoplatystoma corruscans in the São Francisco Basin, Brazil. Dis. Aquat. Org. 107: 211-221. Go to original source... Go to PubMed...
  29. Posada D. 2008: jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 25: 1253-1256. Go to original source... Go to PubMed...
  30. Prunescu C.C., Prunescu P., Pucek Z., Lom J. 2007: The first finding of myxosporean development from plasmodia to spores in terrestrial mammals: Soricimyxum fegati gen. sp n. (Myxozoa) from Sorex araneus (Soricomorpha). Folia Parasitol. 54: 159-164. Go to original source... Go to PubMed...
  31. Rambaut. 2008: FigTree v1.1.1: Tree figure drawing tool. http:// tree.bio.ed.ac.uk/software/figtree/ (accessed 7/2014).
  32. Sato Y., Fenerich-Verani., Godinho H.P. 2003: Reprodução induzida de peixes da bacia do São Francisco. In: H.P. Godinho and A.L. Godinho (Eds), Águas, Peixes e Pescadores do São Francisco das Minas Gerais. Belo Horizonte, PUC Minas, pp. 275-289.
  33. Shin S.P., Nguyen V.G., Jeong J.M., Jun J.W., Kim J.H., Jan J.E., Baeck G.W., Park S.C. 2014: The phylogenetic study on Thelohanellus species (Myxosporea) in relation to host specificity and infection site tropism. Mol. Phyl. Evol. 72: 31-34. Go to original source... Go to PubMed...
  34. Swofford D.L. 1998: PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Ver. 4. Sinauer Associates, Sunderland, MA.
  35. 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. Mol. Biol. Evol. 28: 2731-2739. Go to original source... Go to PubMed...