Skip to main content
SpringerLink
Log in

Myxobolus turpisrotundus (Myxosporea: Bivalvulida) spores with caudal appendages: investigating the validity of the genus Henneguya with morphological and molecular evidence

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

Abstract

Spores of the myxozoan parasite Myxobolus turpisrotundus Zhang 2009 were observed for the first time bearing caudal appendages. Most spores had the typical Myxobolus spp. morphology, but approximately 10% of spores possessed a spore body that was slightly elongated with a short tail projecting from the spore valve. In other spores, the tail was much more clearly visible and elongate. The spore body of these unusual spores is consistent in morphology and dimension to the normal spores of M. turpisrotundus. Both spore types were found within individual cysts, and the small subunit ribosomal RNA (ssrRNA) gene sequence from parasite cysts of this type was nearly identical to the previously published sequence of M. turpisrotundus from allogynogenetic gibel carp Carassius auratus gibelio (Bloch). The phenomenon of Myxobolus spores with caudal appendages provides additional evidence that the use of this character to separate Myxobolus and Henneguya into distinct genera is not reflective of an evolutionarily accurate classification scheme. Phylogenetic analysis of ssrDNA sequence from Myxobolus and Henneguya species showed clustering of species in some locations of the tree, but ultimately these genera are intermixed. The use of a single character to delineate species in the two most species-rich myxozoan genera has been consistently challenged where DNA analyses are used. The present finding of a single species bearing both Myxobolus-type and Henneguya-type spores emphasizes the inadequacy of this classification scheme, and highlights the need for careful consideration of these variable characteristics when describing myxozoan species.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Al Quraishy S, Koura E, Abdel-Baki A, Bashtar AR, El Deed N, Al Rasheid K, Abdel Ghaffar F (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

    Article  CAS  PubMed  Google Scholar 

  • Andree KB, Székely C, Molnár K, Gresoviac SJ, Hedrick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bilvalvulidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74

    Article  CAS  PubMed  Google Scholar 

  • 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 

  • Bahri S, Andree KB, Hedrick RP (2003) Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol 50:417–424

    Article  Google Scholar 

  • Bartošova P, Fiala I, Hypša V (2009) Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide an effective tool for their molecular phylogenetics. Mol Phylogenet Evol 53:81–93

    Article  PubMed  Google Scholar 

  • Cuadrado M, Albinyana G, Padrós F, Redondo MJ, Sitjà-Bobadilla A, Álvarez-Pellitero P, Palenzuela O, Diamant A, Crespo S (2007) An unidentified epi-epithelial myxosporean in the intestine of gilthead sea bream Sparus aurata L. Parasitol Res 101:403–411

    Article  CAS  PubMed  Google Scholar 

  • Eiras JC (2002) Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 52:43–54

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Eiras JC, Takemoto RM, Pavanelli GC (2009) Henneguya corruscans n. sp. (Myxozoa, Myxosporea, Myxobolidae), a parasite of Pseudoplatystoma corruscans (Osteichthyes, Pimelodidae) from the Paraná River, Brazil: a morphological and morphometric study. Vet Parasitol 159:154–158

    Article  CAS  PubMed  Google Scholar 

  • El-Mansy A (2005) Revision of Myxobolus heterosporus Baker, 1963 (syn. Myxosoma heterospora) (Myxozoa: Myxosporea) in African records. Dis Aquat Org 63:205–214

    Article  CAS  PubMed  Google Scholar 

  • Eszterbauer E, Benko M, Dan A (2001) Identification of fish parasitic Myxobolus (Myxosporea) species using a combined PCR-RFLP method. Dis Aquat Org 44:35–39

    Article  CAS  PubMed  Google Scholar 

  • Ferguson JA, Atkinson SD, Whipps CM, Kent ML (2008) Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of Myxobolus fryeri n. sp. J Parasitol 94:1322–1334

    Article  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704

    Article  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Jirků M, Fiala I, Modrý D (2007) Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology 134:1727–1739

    PubMed  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 

  • Liu Y, Gu ZM, Luo YL (2010) Some additional data to the occurrence, morphology and validity of Myxobolus turpisrotundus Zhang, 2009 (Myxozoa: Myxosporea). Parasitol Res. doi:10.1007/s00436-010-1835-9

    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 (1992) Fine structure of Triactinomyxon early stages and sporogony: Myxosporean and Actinosporean features compared. J Protozool 39:16–27

    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

    PubMed  Google Scholar 

  • Lom J, Noble ER (1984) Revised classification of the class Myxosporea Bütschli, 1881. Folia Parasitol 31:193–205

    Google Scholar 

  • McConnell CJ, Cone DK (1992) Settling rates and density of spores of Henneguya doori (Myxosporea) in water. J Parasitol 78:427–429

    Article  CAS  PubMed  Google Scholar 

  • Molnár K, Eszterbauer E, Székely C, Dan A, Harrach B (2002) Morphological and molecular biological studies on intramuscular Myxobolus spp. of cyprinid fish. J Fish Dis 25:643–652

    Article  Google Scholar 

  • Molnár K, Marton S, Eszterbauer E, Székely C (2006) Comparative morphological and molecular studies on Myxobolus spp. infecting chub from the River Danube, Hungary, and description of M. muellericus sp. n. Dis Aquat Org 73:49–61

    Article  PubMed  Google Scholar 

  • Molnár K, Székely C, Hallett SL, Atkinson SD (2009) Some remarks on the occurrence, host-specificity and validity of Myxobolus rotundus Nemeczek, 1911 (Myxozoa: Myxosporea). Syst Parasitol 72:71–79

    Article  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Shulman SS (1966) Myxosporidia of the Fauna of the USSR. Nauka, Moscow (in Russian)

    Google Scholar 

  • Smothers JF, Von Dohlen CD, Smith LH, Spall RD (1994) Molecular evidence that the myxozoan protists are metazoans. Science 265:1719–1721

    Article  CAS  PubMed  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. Nucl Acids Res 25:4876–4882

    Article  CAS  PubMed  Google Scholar 

  • Whipps CM, Diggles BK (2006) Kudoa alliaria in flesh of Argentinian Hoki Macruronus magellanicus (Gadiformes; Merlucciidae). Dis Aquat Org 69:259–263

    Article  PubMed  Google Scholar 

  • Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53:364–474

    Article  CAS  PubMed  Google Scholar 

  • Whipps CM, El-Matbouli M, Hedrick RP, Blazer V, Kent ML (2004) Myxobolus cerebralis internal transcribed spacer 1 (ITS-1) sequences support recent spread of the parasite to North America and within Europe. Dis Aquat Org 60:105–108

    Article  CAS  PubMed  Google Scholar 

  • 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 28:479–487

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This study was supported by grants of the Natural Science Foundation of Hubei Province (2008CDB078) and Huazhong Agricultural University Scientific and Technological Self-innovation Foundation (2009SC017).

Author information

Authors and Affiliations

  1. Key Lab of Freshwater Biodiversity Conservation and Utilization, Ministry of Agriculture, College of Fisheries, Huazhong Agricultural University, Wuhan, Hubei province, 430070, People’s Republic of China

    Yang Liu & Z. M. Gu

  2. SUNY-ESF, State University of New York College of Environmental Science and Forestry, Environmental and Forest Biology, 246 Illick Hall, 1 Forestry Drive, Syracuse, NY, 13210, USA

    Christopher M. Whipps

  3. Research Institute of Haid Group Co., Ltd. (HIR), Wuhan, Hubei province, 430070, People’s Republic of China

    Yang Liu & Z. M. Gu

  4. Key Lab of Freshwater Biodiversity Conservation and Utilization, Ministry of Agriculture, Yangtze River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Jingzhou City, Hubei, 434000, People’s Republic of China

    L. B. Zeng

Authors
  1. Yang Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christopher M. Whipps
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Z. M. Gu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. L. B. Zeng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Z. M. Gu.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, Y., Whipps, C.M., Gu, Z.M. et al. 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 (2010). https://doi.org/10.1007/s00436-010-1924-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-010-1924-9

Keywords

Search

Navigation