Acta Parasitologica

, Volume 63, Issue 2, pp 221–231 | Cite as

Morphological, histological and molecular characterization of Myxobolus kingchowensis and Thelohanellus cf. sinensis infecting gibel carp Carassius auratus gibelio (Bloch, 1782)

  • Bo Zhang
  • Yanhua Zhai
  • Zemao Gu
  • Yang LiuEmail author


A Myxobolus species and a Thelohanellus species infecting Carassius auratus gibelio (Bloch, 1782) were redescribed by their morphological, histological and molecular characterization. In the present study, the Myxobolus species infecting the muscle was identified as Myxobolus kingchowensis Chen et Ma, 1998 by the morphological and molecular data. Histologically, mature spores of M. kingchowensis were observed in the intercellular and connective tissue of muscle, though the plasmodia were not found. In addition, scattered spores also occurred in the intercellular of haematopoietic cells, intraepithelial of the renal tubules and interior of the melano-macrophage centres. Phylogenetic analysis showed that M. kingchowensis clustered in the clade of muscle-infecting Myxobolus species, further supporting muscle as the infection site of M. kingchowensis. The present Thelohanellus species infecting the gills was identified conspecific as Thelohanellus sinensis reported in Sun (2006) (mark it as T. sinensis-Sun) based on spore morphology, biological traits (host specificity and organ specificity), and molecular data. However, compared with the original description of T. sinensis Chen et Hsieh, 1960, the present Thelohanellus species and T. sinensis-Sun both infecting the gills of gibel carp are distinguishable from the original description in the host and infection site, which made the validity of T. sinensis-Sun dubious. Due to the absence of molecular data in the original description of T. sinensis, we suggest marking the present species and T. sinensis-Sun as T. cf. sinensis to avoid the confusion until T. sinensis is obtained from the type host and type infection site.


Myxosporea Myxobolus kingchowensis Thelohanellus sinensis Carassius auratus gibelio China 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Atkinson, S.D., Bartošová-Sojková P., Whipps, C.M., Bartholomew J.L. 2015. Approaches for characterising myxozoan species. (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 111–123. DOI: Scholar
  2. Chen C.L. 1973. An illustrated guide to the fish diseases and causative pathogenic fauna and flora in the Hubei Province. Inst. Hydrobiol., Publishing House Science, Beijing, China. (In Chinese)Google Scholar
  3. Chen, C.L., Hsieh S.R. 1960. Studies on sporozoa from the freshwater fishes Ophiocephalus maculatus and O. argus of China. Actc Hydrobiologica Sinica, 2, 171–196Google Scholar
  4. Chen, Q.L., Ma C.L. 1998. Myxozoa: Myxosporea. Science Press, Beijing. (In Chinese)Google Scholar
  5. Darriba, D., Taboada, G.L., Doallo, R., Posada D. 2012. jModelTest 2: more models, new heuristics and parallel computing. Nature Methods, 9, 772–772. DOI: 10.1038/nmeth.2109CrossRefGoogle Scholar
  6. Dereeper, A., Audic, S., Claverie J.-M., Blanc G. 2010. BLAST-EXPLORER helps you building datasets for phylogenetic analysis. BMC Evolutionary Biology, 10, 8. DOI: Scholar
  7. Dereeper, A., Guignon, V., Blanc, G., Audic, S., Buffet, S., Chevenet, F., et al. 2008. Phylogeny. fr: robust phylogenetic analysis for the non-specialist. Nucleic Acids Research, 36, W465–W469. DOI: Scholar
  8. Drummond, A.J., Rambaut A. 2007. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology, 7, 214. DOI: Scholar
  9. Eiras, J.C., Molnár, K., Lu Y.S. 2005. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 61, 1–46. DOI: 10.1007/s11230-004-6343-9CrossRefGoogle Scholar
  10. Fiala, I., Bartošová-Sojková P., Whipps C.M. 2015. Classification and phylogenetics of Myxozoa. (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 85–110. DOI: Scholar
  11. 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/syq010CrossRefGoogle Scholar
  12. Guindon, S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696–704. DOI: 10.1080/10635150390235520CrossRefGoogle Scholar
  13. Hartigan, A., Wilkinson, M., Gower, D.J., Streicher, J.W., Holzer, A.S., Okamura B. 2016. Myxozoan infections of caecilians demonstrate broad host specificity and indicate a link with human activity. International Journal for Parasitology, 46, 375–381. DOI: Scholar
  14. Hillis, D.M., Dixon M.T. 1991. Ribosomal DNA: molecular evolution and phylogenetic inference. The Quarterly Review of Biology, 66, 411–453. DOI: Scholar
  15. Katoh, K., Standley D.M. 2013. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution, 30, 772–780. DOI: 10.1093/molbev/mst010CrossRefGoogle Scholar
  16. Kent, M.L., Bagshaw, J.W., Nener, J., Raymond B. 1996. Myxobolus cyprini Doflein, 1898, in Peamouth: First Report of This Myxosporean in the Western Hemisphere. Journal of Aquatic Animal Health, 8, 159–162. DOI: 10.1577/1548-8667 (1996) 008< 0159: MCDIPF>2.3.CO;2CrossRefGoogle Scholar
  17. Liu, Y., Zhai, Y.H., Gu Z.M. 2016b. Morphological and molecular characterization of Thelohanellus macrovacuolaris n. sp. Myxosporea: Bivalvulida infecting the palate in the mouth of common carp Cyprinus carpio L. in China. Parasitology International, 65, 303–307. DOI: Scholar
  18. Lom, J., Arthur J. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156. DOI: 10.1111/j.1365-2761.1989. tb00287.xCrossRefGoogle Scholar
  19. Maciel, P.O., Affonso, E.G., Boijink C.D.L., Tavaresdias, M., Inoue L.A.K.A. 2011. Myxobolus sp. (Myxozoa) in the circulating blood of Colossoma macropomum (Osteichthyes, Characidae). Revista Brasileira De Parasitologia Veterinaria, 20, 82–84. DOI: 10.1590/S1984-29612011000100018CrossRefGoogle Scholar
  20. Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitology Hung, 27, 5–20Google Scholar
  21. Molnár K. 2011. Remarks to the validity of Genbank sequences of Myxobolus spp. Myxozoa, Myxosporidae infecting Eurasian fishes. Acta Parasitologica, 56, 263. DOI: Scholar
  22. Molnár, K., Eszterbauer E. 2015. Specificity of infection sites in vertebrate hosts. In: (Eds B. Okamura, A. Gruhl, J. L. Bartholomew) Myxozoan Evolution, Ecology and Development, Cham, Springer. pp. 295–313. DOI: 319-14753-6_16CrossRefGoogle Scholar
  23. Molnár, K., Kovács-Gayer É. 1985. The pathogenicity and development within the host fish of Myxobolus cyprini Doflein, 1898. Parasitology, 90, 549–555. DOI: 10.1017/S0031182000055530CrossRefGoogle Scholar
  24. Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., et al. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. DOI: Scholar
  25. Sun C.Y. 2006. Morphological and molecular comparison of myxosporeans. Master Thesis, Chong Qing Normal University, Chongqing, China. (In Chinese)Google Scholar
  26. Whipps, C.M., Adlard, R.D., Bryant, M.S., Lester, R.J., Findlay, V., Kent M.L. 2003. First report of three Kudoa species from eastern Australia: Kudoa thyrsites from mahi mahi Coryphaena hippurus, Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper Pempheris ypsilychnus. Journal of Eukaryotic Microbiology, 50, 215–219. DOI: 10.1111/j.1550-7408.2003.tb00120.xCrossRefGoogle Scholar
  27. Yuan, S., Xi, B., Wang, J., Xie, J., Zhang J. 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. Parasitology Research, 114, 37–45. DOI: Scholar
  28. Zhang, J.Y., Gu, Z.M., Kalavati, C., Eiras, J.C., Liu, Y., Guo, Q.Y., et al. 2013. Synopsis of the species of Thelohanellus Kudo, 1933 (Myxozoa: Myxosporea: Bivalvulida). Systematic Parasitology, 86, 235–256. DOI: 10.1007/s11230-013-9449-0CrossRefGoogle Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2018

Authors and Affiliations

  1. 1.Department of Aquatic Animal Medicine, College of FisheriesHuazhong Agricultural UniversityWuhanPeople’s Republic of China
  2. 2.Hubei Engineering Research Center for Aquatic Animal Diseases Control and PreventionWuhanPeople’s Republic of China

Personalised recommendations