Skip to main content
Log in

Molecular genetic studies on morphologically indistinguishable Myxobolus spp. infecting cyprinid fishes, with the description of three new species, M. alvarezae sp. nov., M. sitjae sp. nov. and M. eirasianus sp. nov.

  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

While studying Myxobolus gill infections of cyprinid fishes, the authors found large, segmented plasmodia in three species: ide (Leuciscus idus), asp (Aspius aspius) and white bream (Blicca bjoerkna). As regards their size and morphology, the spores from these plasmodia corresponded to those of M. dujardini described from chub (Leuciscus cephalus). However, the 18S rDNA sequences of spores from the three cyprinids differed from those of M. dujardini. Based on molecular differences, this paper describes two new species: M. alvarezae sp. nov. from ide and asp, and M. sitjae sp. nov. from white bream. The two new species and M. dujardini had a similar tissue tropism, and infected the multilayered epithelium of the gill filaments. Histological examination of the infected filaments demonstrated that the large plasmodia with multiple buddings were formed from amalgamating small plasmodia. Besides carrying infection in the filamental epithelium, the three above fish species were infected by small intralamellar plasmodia as well. These plasmodia were filled by spores that resembled the roach parasite M. intimus both in morphology and seasonal development. The 18S rDNA sequences of ‘intimus-like’ spores from ide and asp differed only in some base pairs from spores found in the type host roach, and were identified as belonging to M. intimus. The spores found in white bream, however, showed 3.6-5.0% difference in DNA sequence from those of M. intimus; therefore, they have been described as M. eirasianus sp. nov. The aim of this paper was to demonstrate the importance of using molecular methods for separating and identifying morphologically corresponding or closely similar Myxobolus spp.

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.

Similar content being viewed by others

References

  • Andree K.B., El-Matbouli M., Hoffmann R.W., Hedrick R.P. 1999. Comparison of 18S rDNA sequences of selected geographic isolates of Myxobolus cerebralis. International Journal of Parasitology, 29, 771–775. DOI: 10.1016/S0020-7519(99) 00035-1.

    Article  PubMed  CAS  Google Scholar 

  • Barta J.R., Martin D.S., Liberator P.A., Dashkevicz M., Anderson J.W., Feighner S.D., Elbrecht A., Perkins-Barrow A., Jenkins M.C., Danforth H.D., Ruff M.D., Profous-Juchelka H. 1997. Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology, 83, 262–271. DOI: 10.2307/3284453.

    Article  PubMed  CAS  Google Scholar 

  • Briolay J., Galtier N., Brito R.M., Bouvet Y. 1998. Molecular phylogeny of Cyprinidae inferred from cytochrome b DNA sequences. Molecular Phylogenetics and Evolution, 9, 100–108. DOI: 10.1006/mpev.1997.0441.

    Article  PubMed  CAS  Google Scholar 

  • Cone D.K., Overstreet R.M. 1998. Species of Myxobolus (Myxozoa) from the bulbus arteriosus of centrarchid fishes in North America, with a description of two new species. Journal of Parasitology, 84, 371–374. DOI: 10.2307/3284499.

    Article  PubMed  CAS  Google Scholar 

  • Costedoat C., Chappaz R., Barascud B., Guillard O., Gilles A. 2006. Heterogeneous colonization pattern of European cyprinids, as highlighted by the dace complex (Teleostei: Cyprinidae). Molecular Phylogenetics and Evolution, 41, 128–148. DOI: 10.1016/j.ympev.2006.04.022.

    Article  Google Scholar 

  • Donec Z.S., Shulman S.S. 1984. Cnidosporidia. In: (Ed. Bauer O.N.) Key to the parasites of freshwater fishes of the USSR. Vol. 1. Nauka, Leningrad, 88–251 (in Russian).

    Google Scholar 

  • Dyková I., Lom J. 2007. Histopathology of protistan and myxozoan infections in fishes. An Atlas. Academia, Praha, 219 pp.

    Google Scholar 

  • Eiras J.C., Molnár K., Lu Y.S. 2005. Synopsis of the genus Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 61, 1–46. DOI: 10.1007/s11230-004-6343-9.

    Article  PubMed  CAS  Google Scholar 

  • Eszterbauer E. 2002. Molecular biology can differentiate morphologically indistinguishable myxosporean species: Myxobolus elegans and M. hungaricus. Acta Veterinaria Hungarica, 50, 59–62. DOI: 10.1556/AVet.50.2002.1.8.

    Article  PubMed  Google Scholar 

  • Eszterbauer E. 2004. Genetic relationship among gill-infecting Myxobolus species (Myxosporea) of cyprinids: molecular evidence of importance of tissue-specificity. Diseases of Aquatic Organisms, 58, 35–40. DOI: 10.3354/dao058035.

    Article  PubMed  Google Scholar 

  • Eszterbauer E., Szekely Cs. 2004. Molecular phylogeny of the kidney-parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica, 52, 469–478. DOI: 10.1046/j.1365-2761.2002.00409.x.

    Article  PubMed  CAS  Google Scholar 

  • Feist S.W., Longshaw M. 2006. Phylum Myxozoa. In: (Ed. Wu P.T.K.) Fish diseases and disorders: Protozoan and metazoan infections. Vol. 1. Second edition. CAB International, Oxfordshire, pp. 23–296.

    Google Scholar 

  • Hall T.A. 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    CAS  Google Scholar 

  • 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. Diseases of Aquatic Organisms, 46, 197–212.

    Article  PubMed  CAS  Google Scholar 

  • Hedrick R.P., McDowell T.S., Mukkatira K., Georgiadis M.P., Mac-Connel E. 1999. Susceptibility of selected inland salmonids to experimentally induced infections with Myxobolus cerebralis, the causative agent of whirling disease. Journal of Aquatic Animal Health, 11, 330–339. DOI: 10.1577/1548-8667(1999)011.

    Article  Google Scholar 

  • Hedrick R.P., McDowell T.S., Mukkatira K., Georgiadis M.P., Mac-Connel E. 2001. Susceptibility of three species of anadromous salmonids to experimentally induced infectious with Myxobolus cerebralis, the causative agent of whirling disease. Journal of Aquatic Animal Health, 13, 43–50. DOI: 10.1577/1548-8667(2001)013<0043:SOTSOA>2.0.CO;2.

    Article  Google Scholar 

  • Huelsenbeck J.P., Ronquist F. 2001. MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics, 17, 754–755. DOI: 10.1093/bioinformatics/17.8.754.

    Article  PubMed  CAS  Google Scholar 

  • Lom J. 1961. Protozoan parasites found in Czechoslovakian fishes I. Folia Zoologica, 10, 45–56.

    Google Scholar 

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

    PubMed  Google Scholar 

  • Masoumian M., Baska F., Molnár K. 1996. Myxobolus nodulointestinalis sp. n. (Myxosporea, Myxobolidae), a parasite of the intestine of Barbus sharpeyi. Diseases of Aquatic Organisms, 24, 35–39. DOI: 10.3354/dao024035.

    Article  Google Scholar 

  • Milne I., Lindner D., Bayer M., Husmeier D., McGuire G., Marshall D.F., Wright F. 2008. TOPALi v2: as rich graphical interface for evolutionary analyses of multiple alignments on HPC clusters and multi-core desktops. Bioinformatics, 25, 126–127. DOI: 10.1093/bioinformatics/btn575.

    Article  PubMed  Google Scholar 

  • Molnár K. 1994. Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologia Hungarica, 27, 5–20.

    Google Scholar 

  • Molnár K., Eszterbauer E., Székely Cs., Dán Á., Harrach B. 2002. Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. Journal of Fish Diseases, 25, 643–652. DOI: 10.1046/j.1365-2761.2002.00409.x.

    Article  Google Scholar 

  • Molnár K., Marton Sz., Eszterbauer E., Székely Cs. 2006. Comparative morphological and molecular studies on Myxobolus spp. infecting chub from the River Danube, Hungary, and description of M. muellericus sp. n. Diseases of Aquatic Organisms, 73, 49–61. DOI: 10.3354/dao073049.

    Article  PubMed  Google Scholar 

  • Molnár K., Marton Sz., Székely Cs., Eszterbauer E. 2010. Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitology Research, 107, 1137–1150. DOI: 10.1007/s00436-010-1982-z.

    Article  PubMed  Google Scholar 

  • Perea S., Böhme M., Żupančič P., Freyhof J., Šanda R., Ozuluğ M., Abdoli A., Doadrio I. 2010. Phylogenetic relationships and biogeographical patterns in Circum-Mediterranean subfamily Leuciscinae (Teleostei, Cyprinidae) inferred from both mitochondrial and nuclear data. BMC Evolutionary Biology, 10, 265. DOI: 1186/1471-2148-10-265.

    Article  PubMed  Google Scholar 

  • Posada D. 2008. jModelTest: phylogenetic model averaging. Molecular Biology and Evolution, 25, 1253–1256. DOI: 10.1093/msn083.

    Article  PubMed  CAS  Google Scholar 

  • Rácz O.Z., Székely Cs., Molnár K. 2004. Intraoligochaete development of Myxobolus intimus (Myxosporea: Myxobolidae), a gill myxosporean of the roach (Rutilus rutilus). Folia Parasitologica, 51, 199–207.

    PubMed  Google Scholar 

  • 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. Molecular Biology and Evolution, 28, 2731–2739. DOI: 10.1093/molbev/msr121.

    Article  PubMed  CAS  Google Scholar 

  • Thélohan P. 1892. Observation sur les myxosporidies et essai de classification de ces organismes. Bulletin de la Société Philomathique de Paris, 4, 165–178.

    Google Scholar 

  • Thompson J.D., Higgins D.G., Gibson T.J. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research, 2, 4673–4680. DOI: 10.1093/nar/22.22.4673.

    Article  Google Scholar 

  • Urawa S., Freeman M.A., Johnson S.C., Jones S.R.M., Yokoyama H. 2011. Geographical variation in spore morphology, gene sequences, and host specificity of Myxobolus arcticus (Myxozoa) infecting salmonid nerve tissues. Diseases of Aquatic Organisms, 96, 229–237. DOI: 10.3354/dao02398.

    Article  PubMed  Google Scholar 

  • Zardoya R., Doadrio I. 1999. Molecular evidence on the evolutionary and biogeographical patterns of European cyprinids. Journal of Molecular Evolution, 9, 227–237. DOI: 10.1007/PL00006545.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Gábor Cech.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cech, G., Molnár, K. & Székely, C. Molecular genetic studies on morphologically indistinguishable Myxobolus spp. infecting cyprinid fishes, with the description of three new species, M. alvarezae sp. nov., M. sitjae sp. nov. and M. eirasianus sp. nov.. Acta Parasit. 57, 354–366 (2012). https://doi.org/10.2478/s11686-012-0045-2

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.2478/s11686-012-0045-2

Keywords

Navigation