Advertisement

Parasitology Research

, Volume 118, Issue 12, pp 3327–3336 | Cite as

A new myxozoan species Henneguya unitaeniata sp. nov. (Cnidaria: Myxosporea) on gills of Hoplerythrinus unitaeniatus from Mato Grosso State, Brazil

  • Letícia Pereira ÚngariEmail author
  • Diego Henrique Mirandola Dias Vieira
  • Reinaldo José da Silva
  • André Luiz Quagliatto Santos
  • Rodney Kozlowiski de Azevedo
  • Lucia Helena O’Dwyer
Fish Parasitology - Original Paper

Abstract

On the basis of morphological and molecular analyses, a new myxozoan parasite is described from the gills of the fish Hoplerythrinus unitaeniatus, collected in the municipality of Nova Xavantina, Mato Grosso State, Brazil. Plasmodia of Henneguya unitaeniata sp. nov. were oval and whitish and were found surrounded by collagen fibers forming plasmodia wall between gill filaments on the gill arch. The spores were ellipsoidal with two similar polar capsules. Morphometric analysis showed a total spore mean length of 23.8 ± 1.5 μm, spore body mean length of 14.5 ± 0.7 μm, caudal appendage mean length of 10.3 ± 1.4 μm, thickness mean length of 4.3 ± 0.3 μm, polar capsule mean length of 4.2 ± 0.5 μm, polar capsule mean width of 1.8 ± 0.3 μm, spore mean width of 4.8 ± 0.4 μm, and 4–5 polar filament coils. Phylogenetic analysis showed Henneguya unitaeniata sp. nov. as a basal species in a subclade formed by myxozoans that parasitize bryconid fishes.

Keywords

Erythrinidae Histopathology Myxobolidae Phylogeny SSU rDNA 

Notes

Acknowledgments

We thank the team of the Laboratory for Teaching and Research in Wild Animals (LAPAS-UFU) for their assistance in the fish collection. R.J.S. is supported by FAPESP #2016/50377-1; CNPq #309125/2017-0; CNPq-PROTAX #440496/2015-2.

Funding information

We are grateful to FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo) and FAPEMIG (Fundação de Amparo à Pesquisa do Estado de Minas Gerais) for financial support.

Compliance with ethical standards

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed (IBAMA license 60640-1).

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Abdallah VD, Azevedo RK, Luke JL, Bonfim TCB (2007) Two new species of Henneguya Thélohan, 1892 (Myxozoa, Myxobolidae), parasitic on the gills of Hoplosternum littorale (Callichthyidae) and Cyphocharax gilbert (Curimatidae) from the Guandu River, State of Rio de Janeiro, Brazil. Parasitol Latinoam 62:35-41Google Scholar
  2. Abrunhosa J, Sindeaux-Neto JL, Hamoy I, Matos ER (2018) A new species of Myxosporea, Henneguya quelen, from silver catfish Rhamdia quelen (Siluriforme: Pimelodidae) in Amazonian region. Parasitol Res 117:3809–3820.  https://doi.org/10.1590/s1984-29612017067 CrossRefPubMedGoogle Scholar
  3. Adriano EA, Arana S, Cordeiro NS (2005) An ultrastructural and histophatological study of Henneguya pellucida n. sp. (Myxosporea: Myxobolidae) infecting Piaractus mesopotamicus (Characidae) cultivated in Brazil. Parasite 12:221–227.  https://doi.org/10.1051/parasite/2005123221 CrossRefPubMedGoogle Scholar
  4. Alcântara NM, Tavares-Dias M (2015) Structure of the parasites communities in two Erythrinidae fish from Amazon river system (Brazil). Braz J Vet Parasitol 24:189–190.  https://doi.org/10.1590/S1984-29612015039 CrossRefGoogle Scholar
  5. Alvarez-Pellitero P, Palenzuela O, Sitjà-Bobadilla A (2008) Histopathology and cellular response in Enteromyxum leei (Myxozoa) infections of Diplodus puntazzo (Teleostei). Parasitol Int 57:110–120.  https://doi.org/10.1016/j.parint.2007.09.004 CrossRefPubMedGoogle Scholar
  6. Andree KB, Székely C, Molnár K, Gresoviac SJ, Hedrick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa : Bilvalvidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74.  https://doi.org/10.2307/3285702 CrossRefPubMedGoogle Scholar
  7. Azevedo C, Matos E (1995) Henneguya adherens sp. n. (Myxozoa, Myxosporea), parasite of the Amazonian fish, Acestrorhyncus falcatus. J Eukaryot Microbiol 42:515–518CrossRefGoogle Scholar
  8. Azevedo C, Matos E (1996) Henneguya malabarica sp. nov. (Myxozoa, Myxobolidae) in the Amazonian fish Hoplias malabaricus. Parasitol Res 82:222–224CrossRefGoogle Scholar
  9. Azevedo C, Matos E (2002) Fine structure of the myxosporean Henneguya curimata n. sp., parasite of the Amazonian fish, Curimata inormata (Teleostei, Curimatidae). J Eukaryot Microbiol 49:197–200CrossRefGoogle Scholar
  10. Azevedo C, Corral L, Matos E (1997) Light and ultrastructural data on Henneguya testicularis n. sp. (Myxozoa, Myxobolidae), a parasire from the testis of the Amazonian fish Moenkhausia oligolepis. Syst Parasitol 37:111–114CrossRefGoogle Scholar
  11. Azevedo RK, Addallah VD, Paes JVK, Silva RJ, Matos P, Velasco M, Matos E (2013) Henneguya nagelli n. sp. (Myxozoa: Myxobolidae) in Cyphocharax nagelli (Steindachner, 1881) (Teleostei: Characiformes: Curimatidae) from the Peixe’s River, São Paulo State, Brazil. Parasitol Res 112:3601–3605CrossRefGoogle Scholar
  12. Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins-Barrow A, Jenkins MC, Danforth HD, Ruff MD, Profous-Juchelka H (1997) Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. J Parasitol 83:262.  https://doi.org/10.2307/3284453 CrossRefPubMedGoogle Scholar
  13. Bartholomew JL, Atkinson SD, Hallett SL, Lowenstine LJ, Garner MM, Gardiner CH, Rideout BA, Keel MK, Brown JD (2008) Myxozoan parasitism in waterfowl. Int J Parasitol 38:1199–1207.  https://doi.org/10.1016/j.ijpara.2008.01.008 CrossRefPubMedGoogle Scholar
  14. Casal G, Matos E, Azevedo C (2003) Light and ultrastructural aspects of Henneguya striolata sp. nov. (Myxozoa, Myxosporea), a parasite of the Amazonian fish Serrasalmus striolatus. Parasitol Res 83:93–95CrossRefGoogle Scholar
  15. Casal G, Clemente SCS, Leila L, Rocha S, Felizardo N, Oliveira E, Al-Quraishy S, Azevedo C (2017) Ultrastructural morphology and phylogeny of Henneguya gilbert s. sp. (Myxozoa) infecting the teleostean Cyphocharax gilbert (Characiformes: Curimatidae) from Brazil. Parasitol Res 116:2747–2756CrossRefGoogle Scholar
  16. Chambrier A, Scholz T, Vaucher C (1996) Tapeworms (Cestoda: Proteocephalidae) of Hoplias malabaricus (Pisces: Characiformes, Erythrinidae) in Paraguay: description of Proteocephalus regoi sp. n., and redescription of Nomimoscolex matogrossensis. Folia Parasitol 43:133–140Google Scholar
  17. Diamant A, Whipps CM, Kent ML (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.  https://doi.org/10.1645/GE-336R CrossRefPubMedGoogle Scholar
  18. Eiras JC (2002) Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 52:43–54.  https://doi.org/10.1023/A:1015016312195 CrossRefPubMedGoogle Scholar
  19. Eiras JC, Adriano EA (2012) A checklist of new species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012. Syst Parasitol 83:95–104.  https://doi.org/10.1007/s11230-012-9374-7 CrossRefPubMedGoogle Scholar
  20. Eiras JC, Malta JC, Varela A, Pavanelli GC (2004) Henneguya schizodon n. sp. (Myxozoa Myxobolidae), a parasite of the Amazonian teleost fish Schizodon fasciatus (Characiformes, Anostomidae). Parasite 11:169–173.  https://doi.org/10.1051/parasite/2004112169 CrossRefPubMedGoogle Scholar
  21. Eiras JC, Molnár K, Lu YS (2005) Synopsis of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46CrossRefGoogle Scholar
  22. Feist SW, Longshaw M (2006) Phylum Myxozoa. In: Woo PTK (ed) Fish diseases and disorders. Protozoan and metazoan infections. CABI Publishing, Wallingford, pp 230–296Google Scholar
  23. Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36:1521–1534.  https://doi.org/10.1016/j.ijpara.2006.06.016 CrossRefPubMedPubMedCentralGoogle Scholar
  24. Graça W, Pavanelli CS (2007) Peixes de planície de inundação do alto rio Paraná e áreas adjacentes Maringá: EDUEM, 1:241.Google Scholar
  25. Guimarães JRA, Bergamin F (1933) Considerações sobre as ictioepizootias produzidas pelos mixosporídeos do género ‘Henneguya’ Thélohan, 1892 - Henneguya travassoi sp. n. Rev Indust Animal 10:1151–1156Google Scholar
  26. Hall T (2011) BioEdit: an important software for molecular biology. GERF Bull Bisci 2:60–61Google Scholar
  27. Hallett SL, 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.  https://doi.org/10.3354/dao046197 CrossRefPubMedPubMedCentralGoogle Scholar
  28. Jucá-Chagas R (2004) Air breathing of the neotropical fishes Lepidosiren paradoxa, Hoplerythrinus unitaeniatus and Hoplesternum littorale during aquatic hypoxia. Comp Biochem Physiol A 139:49–53.  https://doi.org/10.1016/j.cbpb.2004.06.019 CrossRefGoogle Scholar
  29. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C, Thierer T, Ashton B, Meintjes P, Drummond A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649.  https://doi.org/10.1093/bioinformatics/bts199 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Kent ML, Khattra J, Hervio DML, Devlin RH (1998) Ribosomal DNA sequence analysis of isolates of the PKX Myxosporean and their relationship to members of the genus. J Aquat Anim Health 10:12–12CrossRefGoogle Scholar
  31. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wilm IM, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23(21):2947–2948.  https://doi.org/10.1093/bioinformatics/btm404 CrossRefGoogle Scholar
  32. Lom J, Arthur JR (1989) A guideline for preparation of species descriptions in Myxosporea. K Dish Dis 12:151–156.  https://doi.org/10.1111/j.1365-2761.1989.tb00287.x CrossRefGoogle Scholar
  33. Lom J, Dyková L (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36.  https://doi.org/10.14411/fp.2006.001 CrossRefGoogle Scholar
  34. Lom J, Molnár K (1983) Myxobolus basilamellaris n. sp. (Myxozoa, Myxosporea) parasite of the gills of common carp (Cyprinus carpio L.). Folia Parasitol 30:1–3Google Scholar
  35. Longshaw M, Frear P, Feist SW (2003) Myxobolus buckei sp. n.(Myxozoa), a new pathogenic parasite from the spinal column of three cyprinid fishes from the United Kingdom. Folia Parasitol 50:251–262CrossRefGoogle Scholar
  36. Mariano WS, Oba ET, Santos LRB, Fernandes MN (2009) Respostas fisiológicas de jeju (Hoplerythrinus unitaeniatus) exposto ao ar atmosférico. Rev Bras Saúde Prod Anim 10:210–223Google Scholar
  37. Martins ML, Onaka EM (2006) Henneguya garavelli n. sp. And Myxobolus pecularis n. sp. (Myxozoa: Myxobolidae) in the gills of Cyphocharax nagelli (Osteichthyes: Curimatidae) from Rio de Peixe Reservoir, São José do Rio Pardo, São Paulo. Vet Parasitol 137:253–261CrossRefGoogle Scholar
  38. Martins ML, Souza VN, Moraes JRE, Moraes FR (1999) Gill infection of Leporinus microcephalus Garavello & Britski, 1988 (Myxozoa: Myxobolidae). Description, histophathology and treatment. Ver Brasil Biol 59:527–534CrossRefGoogle Scholar
  39. Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48(3):197–207CrossRefGoogle Scholar
  40. Molnár K, Székely C, Mohamed K, Shaharom-Harrison F (2006) Myxozoan pathogens in cultured Malaysian fishes I. Myxozoan infections of the sutchi catfish Pangasius hypophthalmus in freshwater cage cultures. Dis Aquat Org 68(3):209–218CrossRefGoogle Scholar
  41. Molnár K, Székely C, Guti CF, Eszterbauer E (2014) Two new Myxobolus spp.(Myxozoa: Myxobolidae) from white bream, Blicca bjoerkna (Linnaeus, 1758) developing in basifilamental location of gills. Acta Protozool 53(3):277Google Scholar
  42. Moreira GSA, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2014a) 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.  https://doi.org/10.1007/s00436-014-3815-y CrossRefPubMedGoogle Scholar
  43. Moreira GSA, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2014b) Morphology and 18S rDNA sequencing identifies Henneguya visibilis n sp., a parasite of Leporinus obtusidens from Mogi Guaçu River, Brazil. Parasitol Res 113:81–90.  https://doi.org/10.1007/s00436-013-3629-3 CrossRefPubMedGoogle Scholar
  44. Naldoni J, Arana S, Maia AAM, Ceccarelli PS, Tavares LER, Borges FA, Pozo CF, Adriano EA (2009) Henneguya pseudoplatystoma n. sp. causing reduction in epithelial area of gills in the farmed pintado, a South American catfish: histopathology and ultrastructure. Vet Parasitol 166:52–59.  https://doi.org/10.1016/j.vetpar.2009.07.034 CrossRefPubMedGoogle Scholar
  45. Nemeczek A (1911) Beitrage zur Kenntnis der Myxo und Microsporidien der Fische. Arch Protistenkd 22:143–169Google Scholar
  46. Okamura B, Gruhl A, Bartholomew J (2015) Introduction. In: B. Okamura, A. Gruhl & J.L. Bartholomew (Eds.), Myxozoan evolution, ecology and development. Springer Int Publ 56:1–20Google Scholar
  47. Rambaut A (2012) FigTree v1.4. Molecular evolution, phylogenetics and epidemiology. http://tree.bio.ed.ac.uk/software/figtree/05/2017. Accessed 24 April 2017.
  48. Rocha CAM (2011) Parasitic helminths of the freshwater Neotropical fish Hoplias malabaricus (Characiformes, Erythrinidae) from South America basins. Rev Fish Sci 19(2):150–156.  https://doi.org/10.1080/10641262.2011.557752 CrossRefGoogle Scholar
  49. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  50. Santos GM, Ferreira EJG, Zuanon JAS (2006) Peixes comerciais de Manaus. Ibama/AM; ProVárzea, ManausGoogle Scholar
  51. Soares MGM, Costa EL, Siqueira-Souza F, Anjos HDB, Yamamoto KC, Freitas CEC (2011) Peixes de lagos do médio Rio Solimões, 2nd edn. Instituto Piatam, ManausGoogle Scholar
  52. Thatcher VE (2006) Amazon fish parasites, 2nd edn. Pensoft Publishers, Sofia, p 509Google Scholar
  53. Vieira DHMD, Alama-Bermejo G, Bartholomew JL, Abdallah VD, Azevedo RK (2017) Morphological and molecular discription of Myxobolus batalhensis n. sp. (Myxozoa, Myxosporea), a liver and ovary parasite of Salminus hilarii in Brazil. Parasitol Res 116:3303–3313.  https://doi.org/10.1007/s00436-017-5644-2 CrossRefPubMedGoogle Scholar
  54. Vieira DHMD, Tagliavini VP, Abdallah VD, Azevedo RK (2018) Myxobolus imparfinis n. sp. (Myxozoa: Myxosporea), a new gill parasite of Imparfinis mirini Haseman (Siluriformes: Heptapteridae) in Brazil. Syst Parasitol 95:309–318.  https://doi.org/10.1007/s11230-018-9776-2 CrossRefPubMedGoogle Scholar
  55. Vieira DHMD, Pelegrini LS, Abdallah VD, Azevedo RK (2019) Supplementary studies on Henneguya guanduensis (Cnidaria: Myxosporea) infecting gills and intestine of Hoplosternum littorale in Brazil: ultrastructural and molecular data. Parasitol Int 70:27–32.  https://doi.org/10.1016/j.parint.2019.01.009 CrossRefPubMedGoogle Scholar
  56. Xiao CX, Desser SS (2000) Cladistic analysis of myxozoan species with known alternating life-cycles. Syst Parasitol 46:81–91CrossRefGoogle Scholar
  57. Yokoyama H, Itoh N, Tanaka S (2005) Henneguya pagri n. sp. (Myxozoa: Myxosporea) causing cardiac henneguyosis in red sea bream, Pagrus major (Temminck & Schlegel). J Fish Dis 28(8):479–487.  https://doi.org/10.1111/j.1365-2761.2005.00655.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Letícia Pereira Úngari
    • 1
    Email author
  • Diego Henrique Mirandola Dias Vieira
    • 1
  • Reinaldo José da Silva
    • 1
  • André Luiz Quagliatto Santos
    • 2
  • Rodney Kozlowiski de Azevedo
    • 3
  • Lucia Helena O’Dwyer
    • 1
  1. 1.Universidade Estadual Paulista (Unesp), Departamento de ParasitologiaInstituto de BiociênciasSão PauloBrazil
  2. 2.Laboratório de Ensino e Pesquisa em Animais Silvestres, Faculdade de Medicina VeterináriaUniversidade Federal de UberlândiaUberlândiaBrazil
  3. 3.Centro Universitário CESMACMaceióBrazil

Personalised recommendations