Skip to main content
Log in

Supplemental description and molecular characterization of Myxobolus miyarii Kudo, 1919 (Myxosporea: Myxobolidae) infecting intestine of Amur catfish (Silurus asotus)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Myxobolus miyairii Kudo, 1919 was first reported from the intestines of the Amur catfish (Silurus asotus) in Japan and then in China and Russia, but with incomplete description. During the investigation of fish myxosporean diversity in Poyang Lake, the biggest lake along the Yangtze River, China, two Amur catfish highly infected with M. miyairii in the intestine wall were sampled. So, the complete description of this species with morphological and molecular data was presented here. A large number of whitish, round or ellipsoidal pseudocysts 0.32–0.78 mm in diameter could be found in the external intestinal wall after dissecting the infected fish. Mature spores of M. miyairii were elongated and ellipsoidal in the frontal view and narrow fusiform in the lateral view, with a slightly pointed anterior end and a bluntly rounded posterior end and measured 13.3 ± 0.49 (12.5–14.7) μm × 6.6 ± 0.27 (6.2–7.4) μm × 5.0 ± 0.26 (4.4–5.7) μm in size. Spore surface was smooth and two spore valves symmetrical, with a thin and straight sutural ridge. Interestingly, two types of caudal appendage (single or bifurcated) were occasionally present on the posterior end of some spores which has not previously been reported. The two equal pyriform polar capsules measured 6.5 ± 0.30 (6.2–7.5) μm long and 1.9 ± 0.14 (1.5–2.3) μm wide and situated at the anterior end of the spore. Polar filaments coiled with eight to nine turns, perpendicularly to the longitudinal axis of the polar capsules. Histopathological analysis showed that the plasmodium developed in the circular muscle layer of intestinal wall of Amur catfish, but no obvious inflammatory responses were observed. Phylogenetic analysis based on the partial 18S small subunit ribosomal DNA sequences indicates that M. miyairii cluster within a clade of Siluriforme-infecting Henneguya species with the support of a high bootstrap value, but also evolutionarily independent from the Henneguya clade infecting the epithelium of fish of the Ictaluridae family. Additionally, Myxobolus species reported with caudal processes dispersed within the Henneguya-Myxobolus clade.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Atkinson S, Bartošová P, Whipps CM & Bartholomew JL (2015) Approaches for characterizing myxozoan species in myxozoan evolution, ecology and development, edited by Okamura B, Gruhl A, Bartholomew JL. Springer, ISBN 978–3–319–14753–6 (eBook)

  • Bahri S (2008) Abnormal forms of Myxobolus bizerti and Myxobolus mülleri (Myxosporea: Bivalvulida) spores with caudal appendages. Bull Eur Assoc Fish Pathol 28(6):252–255

    Google Scholar 

  • Barta JR, Martin DS, Liberator PA, Dashkevica 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 83:262–271

    Article  CAS  PubMed  Google Scholar 

  • Baska F, Voronin VN, Eszterbauer E, Muller L, Marton S, Molnár K (2009) Occurrence of two myxosporean species, Myxobolus hakyi sp. n. and Hoferellus pulvinatus sp. n., in Pangasianodon hypophthalmus fry imported from Thailand to Europe as ornamental fish. Parasitol Res 105(5):1391–1398

    Article  PubMed  Google Scholar 

  • Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2013) Molecular phylogeny of the Myxobolus and Henneguya genera with several new south American species. Plos One 8:e73713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen QL, Ma CL (1998) Myxozoa: Myxosporea. Science, Beijing ( In Chinese)

  • Donec ZS, Shulman SS (1984) Parasitic Protozoa. Phylum Cnidosporidia. In: Bauer ON (ed) Key to parasites of freshwater fishes of the USSR, vol 1. Nauka, Leningrad, pp 88–251, In Russian

    Google Scholar 

  • Eiras JC, Molnár K, Lu YS (2005) Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61(1):1–46

    Article  CAS  PubMed  Google Scholar 

  • Eiras JC, Zhang JY, Molnár K (2014) Synopsis of the species of Myxobolus Butschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Syst Parasitol 88(1):11–36

    Article  PubMed  Google Scholar 

  • Eszterbauer E (2004) Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: Molecular evidence of importance of tissue-specificity. Dis Aquat Org 58:35–40

    Article  PubMed  Google Scholar 

  • Evans NM, Holder MT, Barbeitos MS, Okamura B, Cartwright P (2010) The phylogenetic position of Myxozoa: exploring conflicting signals in phylogenomic and ribosomal data sets. Mol Biol Evol 27:2733–2746

    Article  CAS  PubMed  Google Scholar 

  • Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36(14):1521–1534

    Article  CAS  PubMed  Google Scholar 

  • Fiala I, Bartošová P (2010) History of myxozoan character evolution on the basis of rDNA and EF-2 DATA. BMC Evol Biol 10:228

    Article  PubMed  PubMed Central  Google Scholar 

  • Fiala I, Bartošová P, Whipps CM (2015a) Classification and phylogenetics of myxozoa in Myxozoan Evolution, Ecology and Development, edited by Okamura B, Gruhl A, Bartholomew JL. Springer, ISBN 978–3–319–14753–6 (eBook)

  • Fiala I, Bartošová P, Okamura B, Hartikainen H (2015b) Adaptive radiation and evolution within the myxozoa in myxozoan evolution, ecology and development, edited by Okamura B, Gruhl A, Bartholomew JL. Springer, ISBN 978–3–319–14753–6 (eBook)

  • Guindon S, Dufayard JF, 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(3):307–321

    Article  CAS  PubMed  Google Scholar 

  • Hall TA (1999) BioEdit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Sym Ser 41:95–98

    CAS  Google Scholar 

  • Kent ML, Andree KB, Bartholomew JL, El-Matbouli M, Desser SS, Devlin RH, Feist SW, Hedrick RP, Hoffmann RW, Khattra J, Hallett SL, Lester RJG, Longshaw M, Palenzeula O, Siddall ME, Xiao C (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413

    Article  CAS  PubMed  Google Scholar 

  • Kudo R (1919) Illinois biological monographs. 5: p155

  • Liu Y, Whipps CM, Gu ZM, Zeng LB (2010) Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence. Parasitol Res 107:699–706

    Article  PubMed  Google Scholar 

  • Liu Y, Whipps CM, Gu ZM, Huang MJ, He C, Yang HL, Molnár K (2013) Myxobolus musseliusae (Myxozoa: Myxobolidae) from the gills of common carp Cyprinus carpio and revision of Myxobolus dispar recorded in China. Parasitol Res 112:289–296

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Whipps CM, Nie P, Gu ZM (2014) 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

    PubMed  Google Scholar 

  • Lom J, Arthur JR (1989) A guideline for preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156

    Article  Google Scholar 

  • Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53:1–36

    Article  PubMed  Google Scholar 

  • Molnár K (2002) Site preference of fish myxosporeans in the gill. Dis Aquat Org 48:197–207

    Article  PubMed  Google Scholar 

  • Moreira GSA, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (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

    Article  PubMed  Google Scholar 

  • Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12(4):357–358

    CAS  PubMed  Google Scholar 

  • Posada D (2003) Using MODELTEST and PAUP* to select a model of nucleotide substitution. Current Proto Bioinformatics Chapter 6:Unit 6.5

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574

    Article  CAS  PubMed  Google Scholar 

  • Rosser TG, Alberson NR, Baumgartner WA, Mauel MJ, Pote LM, Griffin MJ (2015) Morphological, histological and molecular description of Unicauda fimbrethilae n. sp. (Cnidaria: Myxosporea: Myxobolidae) from the intestinal tract of channel catfish Ictalurus punctatus. J Parasitol (In press)

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30(12):2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The CLUSTAL_X Windows interface: flexible strategies for multiple sequence alignment aided by Quality Analysis Tools. Nucleic Acids Res 25:4876–4883

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Whipps CM, Adlard RD, Bryant MS, Lester RJG, Finflay V, Kent ML (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). J Eukuryot Microbiol 50(3):215–219

    Article  Google Scholar 

  • Zhang JY, Yokoyama H, Wang JG, Li AH, Gong XN, Ryu–Hasegawa A, Iwashita M, Ogawa K (2010) Utilization oftissue habitats by Myxobolus wulii Landsberg & Lom, 1991 in different carp hosts and disease resistance in allogynogenetic gibel carp: redescription of M. wulii from China and Japan. J Fish Dis 33:57–68

    Article  CAS  PubMed  Google Scholar 

  • Zhang JY, Al-Quraishy S, Abdel-Baki AAS (2014) The morphological and molecular characterization of Myxobolus khaliji n. sp. (Myxozoa: Myxosporea) from the double bar seabream Acanthopagrus bifasciatus (Forsskål, 1775) in the Arabian Gulf, Saudi Arabia. Parasitol Res 113:2177–2183

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

The study was partially supported by the Chinese Natural Sciences Fund (31101623, 31411130191, 31472296) and Russian Found of Fundamental Investigation (14–04 = 91176).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Y. Zhang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, X.H., Zhang, J.Y., Batueva, M.D. et al. Supplemental description and molecular characterization of Myxobolus miyarii Kudo, 1919 (Myxosporea: Myxobolidae) infecting intestine of Amur catfish (Silurus asotus). Parasitol Res 115, 1547–1556 (2016). https://doi.org/10.1007/s00436-015-4889-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-015-4889-x

Keywords

Navigation