Folia Parasitologica, vol. 63 (2016)

Folia Parasitologica 63:033 (2016) | DOI: 10.14411/fp.2016.033

Histopathological and ultrastructural studies of Myxobolus turpisrotundus from allogynogenetic gibel carp Carassius auratus gibelio in China

Qingxiang Guo1, Yanhua Zhai1,2,3, Zemao Gu1,2,3, Yang Liu1,2,3
1 Department of Aquatic Animal Medicine, College of Fisheries, Huazhong Agricultural University, Wuhan, China;
2 Key Lab of Freshwater Animal Breeding, Ministry of Agriculture, Wuhan, China;
3 Freshwater Aquaculture Collaborative Innovation Center of Hubei Province, Wuhan, China

During an ongoing systematic survey on species diversity of myxozoans parasitising allogynogenetic gibel carp Carassius auratus gibelio (Bloch) in China, plasmodia were detected in the fins, lip, jaw, gill chamber, gill arches, operculum and oral cavity of infected fish. Combining the morphological and molecular data, the present species was identified as Myxobolus turpisrotundus Zhang, Wang, Li et Gong, 2010. Histopathological examination revealed that despite infecting different organs, M. turpisrotundus always occurred in dermis, demonstrating its affinity to this tissue. Histopathological effect of M. turpisrotundus on the host is relatively mild except parasites in the gill arches producing compression of the adipose tissue and heavy adductor muscles deformation with lymphohistiocytic infiltrates. In addition, the plasmodia in different sites were with the same complex structure arrangement: cup-like cells with unknown derivation, a thin collagenous fibril layer, areolar connective tissue, basement membrane and host epithelial cell. Ultrastructural analysis showed that the parasite has monosporic pansporoblast and sporogenesis followed the usual pattern of most of the myxosporeans.

Keywords: Myxozoan, fish parasites, redescription, tissue affinity, sporogenesis

Received: March 24, 2016; Accepted: August 23, 2016; Published online: October 14, 2016


References

  1. Abdel-Ghaffar F., Abdel-Baki A.A.S., Bayoumy E.M., Bashtar A.R., Al Qurieshy S., Morsey K.S., Alghamdy A., Mehlhorn H. 2008: Light and electron microscopic study on Henneguya suprabranchiae Landsberg, 1987 (Myxozoa: Myxosporea) infecting Oreochromis niloticus, a new host record. Parasitol. Res. 103: 609-617. Go to original source... Go to PubMed...
  2. Abdel-Ghaffar F., Abdel-Aziz A.A.S., Ezz El-Din N., Naas S. 1995: Light and electron microscopic studies on Henneguya branchialis Ashmawy et al 1989 (Myxozoa: Myxosporea) infecting the catfish Clarias lazera in the River Nile, Egypt. J. Union Arab. Biol. 3: 113-133.
  3. Abdel-Ghaffarb F., Abdel-Baki A.A.S., Garhy M.E. 2005: Ultrastructural characteristics of the sporogenesis of genus Myxobolus infecting some Nile fishes in Egypt. Parasitol. Res. 95: 167-171. Go to original source... Go to PubMed...
  4. Adriano E.A., Arana S., Alves A.L., Silva M.R.M., Ceccarelli P.S., Henrique-Silva F., Maia A.A.M. 2009: Myxobolus cordeiroi n. sp., a parasite of Zungaro jahu (Siluriformes: Pimelodidae) from Brazilian Pantanal: morphology, phylogeny and histopathology. Vet. Parasitol. 162: 221-229. Go to original source... Go to PubMed...
  5. Adriano E.A., Arana S., Cordeiro N.S. 2005: An ultrastructural and histopathological study of Henneguya pellucida n. sp. (Myxosporea: Myxobolidae) infecting Piaractus mesopotamicus (Characidae) cultivated in Brazil. Parasite. 12: 221-227. Go to original source... Go to PubMed...
  6. Ali M.A., Abdel-Baki A.S., Sakran T., Entzeroth R., Abdel-Ghaffar F. 2003: Light and electron microscopic studies of Myxobolus stomum n. sp. (Myxosporea: Myxobolidae) infecting the blackspotted grunt Plectorhynicus gaterinus (Forsskål, 1775) in the Red Sea, Egypt. Parasitol. Res. 91: 390-397.
  7. Al Quraishy S., Koura E., Abdel-Baki A.S., Bashtar A.R., El Deed N., Al Rasheid K., Ghaffar F.A. 2008: Light and electron microscopic studies on Kudoa pagrusi sp. n. (Myxosporea: Multivalvulida) infecting the heart of sea bream Pagrus pagrus (L.) from the Red Sea. Parasitol. Res. 102: 205-209. Go to original source... Go to PubMed...
  8. Azevedo C., Matos, E. 1989: Some ultrastructural data on the spore development in a Henneguya sp. parasite of the gill of a Brazilian fish. Parasitol. Res. 76: 131-134. Go to original source... Go to PubMed...
  9. Bartošová-Sojková P., Hrabcová M., Pecková H., Patra S., Kodádková A., Jurajda P., Tyml T., Holzer A.S. 2014: Hidden diversity and evolutionary trends in malacosporean parasites (Cnidaria: Myxozoa) identified using molecular phylogenetics. Int. J. Parasitol. 31: 565-577. Go to original source... Go to PubMed...
  10. Chen Q.L., Ma C.L. (Eds.) 1998: [Myxozoa: Myxosporea.] Science Press, Beijing, 993 pp. (In Chinese.)
  11. Current W.L., Janovy J., 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...
  12. 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...
  13. 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. Parasitol. Res. 88: 617-626. Go to original source... Go to PubMed...
  14. El-Matbouli M., Fischer-Scherl T., Hoffmann R.W. 1990: Light and electron microscopic studies on Myxobolus cotti El-Matbouli and Hoffmann, 1987 infecting the central nervous system of the bullhead (Cottus gobio). Parasitol. Res. 76: 219-227. Go to original source... Go to PubMed...
  15. Food and Agriculture Organization of the United Nations 2014: The State of World Fisheries and Aquaculture. FAO, Rome, 243 pp.
  16. Fishery Bureau in Ministry of Agricultural 2014: [China Fishery Statistics Yearbook.] China Agriculture Press, Beijing, 372 pp. (In Chinese.)
  17. Gui J.F., Zhou L. 2010: Genetic basis and breeding application of clonal diversity and dual reproduction modes in polyploid Carassius auratus gibelio. Sci. China Life Sci. 53: 409-415. Go to original source... Go to PubMed...
  18. 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...
  19. Hillis D.M., Dixon, M.T. 1991: Ribosomal DNA: molecular evolution and phylogenetic inference. Q. Rev. Biol. 66: 411-453. Go to original source... Go to PubMed...
  20. Liu Y., Gu Z.M., Luo Y.L. 2010: Some additional data to the occurrence, morphology and validity of Myxobolus turpisrotundus Zhang, 2009 (Myxozoa: Myxosporea). Parasitol. Res. 107: 67-73. Go to original source... Go to PubMed...
  21. Liu Y., Whipps C.M., Gu Z.M., Zeng C., Huang, M.J. 2012: Myxobolus honghuensis n. sp. (Myxosporea: Bivalvulida) parasitizing the pharynx of allogynogenetic gibel carp Carassius auratus gibelio (Bloch) from Honghu Lake, China. Parasitol. Res. 110: 1331-1336. Go to original source... Go to PubMed...
  22. Liu Y., Whipps C.M., Nie P., Gu Z.M. 2014a: Myxobolus oralis sp. n. (Myxosporea: Bivalvulida) infecting the palate in the mouth of gibel carp Carassius auratus gibelio (Cypriniformes: Cyprinidae). Folia Parasitol. 61: 505-511. Go to original source... Go to PubMed...
  23. Liu Y., Yuan J.F., Jia L., Huang M.J., Zhou Z.G., Gu Z.M. 2014b: Supplemental description of Thelohanellus wuhanensis Xiao et Chen, 1993 (Myxozoa: Myxosporea) infecting the skin of Carassius auratus gibelio (Bloch): ultrastructural and histological data. Parasitol Int. 63: 489-491. Go to original source... Go to PubMed...
  24. Lom J. 1969: Notes on the ultrastructure and sporoblast development in fish parasitizing myxosporidian of the genus Sphaeromyxa. Z. Zellforsch. Mikrosk. Anat. 97: 416-437. Go to original source... Go to PubMed...
  25. Lom J., Arthur J.R. 1989: A guideline for the preparation of species descriptions in Myxosporea. J. Fish Dis. 12: 151-156. Go to original source...
  26. Lu Y., Nie P. 2004: Phylogenetic analyses of the myxosporeans parasitic in freshwater fish of China based on 18S ribosomal DNA. Acta Hydrobiol. Sin. 28: 587-591. (In Chinese with English abstract.)
  27. Manera M., Borreca C., Dezfuli B.S. 2016: Cutaneous myxidiosis in European eel, Anguilla anguilla (Linnaeus, 1758): histopathology, histochemistry and laminin immunohistochemistry. J. Fish Dis. 39: 846-851. Go to original source... Go to PubMed...
  28. Martyn A.A., Hong H., Ringuette M.J., Desser S.S. 2002: Changes in host and parasite-derived cellular and extracellular matrix components in developing cysts of Myxobolus pendula (Myxozoa). J. Eukaryot. Microbiol. 49: 175-182. Go to original source... Go to PubMed...
  29. Molnár K. 1994: Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitol. Hung. 27: 5-20.
  30. Molnár K., Székely C., Hallett S.L., Atkinson S.D. 2009: Some remarks on the occurrence, host-specificity and validity of Myxobolus rotundus Nemeczek, 1911 (Myxozoa: Myxosporea). Syst. Parasitol. 72: 71-79. Go to original source... Go to PubMed...
  31. Morsy K., Semmler M., Al-Olayan E., Mehlhorn H. 2015: Testicular myxosporidiasis and ultrastructural characteristics of Myxobolus bufonis (Myxobolidae) infecting the Egyptian toad Bufo regularis (Bufonidae). A light and electron microscopic study. Parasitol. Res. 114: 3989-3997. Go to original source... Go to PubMed...
  32. Nemeczek A. 1911: Beiträge zur Kenntnis der Myxo- und Microsporidien der Fische. Arch. Protistenk. 22: 143-169.
  33. Okamura B., Gruhl A., Bartholomew J.L. (Eds.), 2015: Myxozoan Evolution, Ecology and Development. Springer International Publishing, Cham, 441 pp.
  34. Pulsford A., Matthews R.A. 1982: An ultrastructural study of Myxobolus exiguus Thelohan, 1895 (Myxosporea) from grey mullet, Crenimugil labrosus (Risso). J. Fish Dis. 5: 509-526. Go to original source...
  35. Wang Z.W., Zhu H.P., Wang D., Jiang F.F., Guo W., Zhou L., Gui, J.F. 2011: A novel nucleo-cytoplasmic hybrid clone formed via androgenesis in polyploid gibel carp. BMC Res. Notes 4: 82. Go to original source... Go to PubMed...
  36. Wu Y.S., Wang J.G. 2000: Studies on the ultrastructure of the sporogenesis of Myxobolus rotundus Nemeczek. Acta Hydrobiol. Sin. 25: 61-69. (In Chinese with English abstract.) Go to original source...
  37. Wu Y.S., Wang J.G. 2003: Structure of the spore of Myxobolus rotundus and Myxobolus guanqiaoensis under optical and scanning electron microscope. Acta Hydrobiol. Sin. 27: 264-268. (In Chinese with English abstract.)
  38. Xi B.W., Xie J., Zhou Q.L., Pan L.K., Ge X.P. 2011: Mass mortality of pond-reared Carassius gibelio caused by Myxobolus ampullicapsulatus in China. Dis. Aquat. Org. 93: 257-260. Go to original source... Go to PubMed...
  39. Ye L.T., Li W.X., Wang W.W., Wu S.G., Wang G.T. 2014: Updated morphology, histopathology and molecular phylogeny of Myxobolus hearti, cardiac Myxosporea in gibel carp, Carassius gibelio (Bloch). J. Fish Dis. 37: 11-20. Go to original source... Go to PubMed...
  40. Yuan S., Xi B.W., Wang J.G., Xie J., Zhang, J.Y. 2015: Thelohanellus wangi n. sp. (Myxozoa, Myxosporea), a new gill parasite of allogynogenetic gibel carp (Carassius auratus gibelio Bloch) in China, causing severe gill myxosporidiosis. Parasitol. Res. 114: 37-45. Go to original source... Go to PubMed...
  41. Zatti S.A., Naldoni J., Silva M.R., Maia A.A., Adriano E.A. 2015: Morphology, ultrastructure and phylogeny of Myxobolus curimatae n. sp. (Myxozoa: Myxosporea) a parasite of Prochilodus costatus (Teleostei: Prochilodontidae) from the São Francisco River, Brazil. Parasitol Int. 64: 362-368. Go to original source... Go to PubMed...
  42. Zhai Y.H., Gu Z.M., Guo Q.X., Wu Z.Z., Wang H.M., Liu Y. 2016: New type of pathogenicity of Thelohanellus kitauei Egusa & Nakajima, 1981 infecting the skin of common carp Cyprinus carpio L. Parasitol Int. 65: 78-82. Go to original source... Go to PubMed...
  43. Zhang J.Y., Gu Z.M., Kalavati C., Eiras J.C., Liu Y., Guo Q.X., Molnár K. 2013: Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Syst. Parasitol. 86: 235-256. Go to original source... Go to PubMed...
  44. Zhang J.Y., Wang J.G., Li A.H., Gong X.N. 2010: Infection of Myxobolus turpisrotundus sp. n. in allogynogenetic gibel carp, Carassius auratus gibelio (Bloch), with revision of Myxobolus rotundus (s. l.) Nemeczek reported from C. auratus auratus (L.). J. Fish Dis. 33: 625-638. Go to original source... Go to PubMed...