Skip to main content

Advertisement

Log in

Morphological and molecular characterization of a new cyprinid gall bladder-infecting Chloromyxum species, Chloromyxum peleci sp. n. (Myxozoa: Chloromyxidae), from Pelecus cultratus (L.) in Russia

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

Abstract

Extensive sampling to get rich data is very important to resolve the current taxonomic problem of Chloromyxum genus and elucidate the nature phylogenetic relationships among congeneric species. During the parasitological survey of cyprinid fish in Gulf of Finland off the coast of St. Petersburg, a new Chloromyxum species, named as Chloromyxum peleci sp. n., was found to infect the gall bladder of sichel, Pelecus cultratus (L.). Here, we provided the morphological, ultrastructural, and molecular features to describe it. Infection was represented by mono- or disporic plasmodia and mature free-floating spores in the gall bladder. Mature spores are typical of freshwater Chloromyxum species, spherical or subspherical in lateral view, measuring 8.8 ± 0.5 μm (7.4–9.5) in length, 7.8 ± 0.3 μm (7.0–8.8) in width, and 7.5 ± 0.4 μm (6.8–8.2) in thickness. Spores have a cog-like appearance in apical view for sutural ridge, and eight to ten widely spaced extrasutural ridges per valve protrude from the spore valve margin. The surface ridge patterns of the new species are similar with those of Chloromyxum auratum and Chloromyxum cristatum, with some branching. Four polar capsules of slightly unequal in two pairs were oval in apical view and pyriform in side view, locating at the anterior end of the spores. Polar filaments coil with four to five turns. The obtained almost full length of 18S ribosomal DNA (rDNA) of Ch. peleci sp. n. does not match any sequences available in GenBank but was most closely related to that of Chloromyxum fluviatile (97.9%). Phylogenetic analysis indicated that Ch. peleci sp. n. clustered in a Chloromyxum subclade infecting the gall bladder of freshwater teleost, with robust nodal support. However, Chloromyxum sensu lato infecting gall bladder of freshwater teleost was again proved to be polyphyletic. The possible evolutionary history of Chloromyxum morphotype of Chloromyxum sensu lato was discussed based on the rDNA-referred phylogeny. This is the second Chloromyxum species from sichel.

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

Access this article

Subscribe and save

Springer+
from $39.99 /Month
  • Starting from 10 chapters or articles per month
  • Access and download chapters and articles from more than 300k books and 2,500 journals
  • Cancel anytime
View plans

Buy Now

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

Similar content being viewed by others

References

  • Abdel-Ghaffar F, Abdel-Gaber R, Maher S, Al Quraishy S, Mehlhorn H (2016) Morphological re-description and molecular characterization of Kudoa pagrusi (Myxosporea: Multivalvulida) infecting the heart muscles of the common sea bream fish Pagrus pagrus (Perciformes: Sparidae) from the Red Sea, Egypt. Parasitol Res 115:3175–3184

    Article  PubMed  Google Scholar 

  • Abdel-Ghaffar F, Abdel-Gaber R, Maher S, Al Quraishy S, Mehlhorn H (2017) Morphological and ultrastructural characteristics of Myxobolus ridibundae n. sp. (Myxosporea: Bivalvulida) infecting the testicular tissue of the marsh frog Rana ridibunda (Amphibia: Ranidae) in Egypt. Parasitol Res 116:133–141

    Article  PubMed  Google Scholar 

  • Barta JR, Martin DS, Liberator PA, Dashkevicz M, Anderson JW, Feighner SD, Elbrecht A, Perkins BA, Jenkins MC, Danforth HD, Ruff MD, Profous JH (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 

  • Bartošová P, Fiala I (2011) Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitol Res 108:573–583

    Article  PubMed  Google Scholar 

  • Bartošová P, Fiala I, Jirků M, Cinková M, Caffara M, Fioravanti ML, Atkinson SD, Bartholomew JL, Holzer AS (2013) Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa). Mol Phylogenet Evol 68:93–105

    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 8:1–12

    Article  Google Scholar 

  • Casal G, Garcia P, Matos P, Monteiro E, Matos E, Azvedo C (2009) Fine structure of Chloromyxum menticirrhi sp.n. (Myxozoa) infecting the urinary bladder of the marine teleost Menticirrhus americanus (Sciaenidae) in Southern Brazil. Euro J Protistol 45:139–146

    Article  Google Scholar 

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

    Google Scholar 

  • Dyková I, Lom J (1988) Chloromyxum reticulatum (Myxozoa, Myxosporea) in the liver of burbot (Lota lota L) and its migration to the final site of infection. Euro J Protistol 23:258–261

    Article  Google Scholar 

  • Eiras JC, Lu YS, Gibson DI, Fiala I, Saraiva A, Cruz C, Santos MJ (2012) Synopsis of the species of Chloromyxum Mingazinni, 1890 (Myxozoa: Myxosporea: Chloromyxidae). Syst Parasitol 83:203–225

    Article  CAS  PubMed  Google Scholar 

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

    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, Dyková I (2004) The phylogeny of marine and freshwater species of the genus Chloromyxum Mingazzini, 1890 (Myxosporea: Bivalvulida) based on small subunit ribosomal RNA gene sequences. Parasitol Res 51:211–214

    CAS  Google Scholar 

  • Fiala I, Bartošová P, Whipps CM (2015) Classification and phylogenetics of Myxozoa. In: Okamura B, Gruhl A, Bartholomew JL (eds) Myxozoan evolution, ecology and development. Springer International Publishing, Cham, pp 85–110

    Chapter  Google Scholar 

  • Gleeson RJ, Adlard RD (2012) Phylogenetic relationships amongst Chloromyxum Mingazzini, 1890 (Myxozoa: Myxosporean), and the description of six novel species from Australian elasmobranchs. Parasitol Int 61:267–274

    Article  CAS  PubMed  Google Scholar 

  • 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 59:307–321

    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 Symp Ser 41:95–98

    CAS  Google Scholar 

  • Hallett SL, Atkinson SD, Holt RA, Banner CR, Bartholomew JL (2006) A new myxozoan form feral goldfish (Carassius auratus). J Parasitol 92:357–363

    Article  PubMed  Google Scholar 

  • Holzer AS, Sommerville C, Wooten R (2006) Molecular identity, phylogeny and life cycle of Chloromyxum schurovi Shul’man & leshko 2003. Parasitol Res 99:90–96

    Article  PubMed  Google Scholar 

  • Holzer AS, Wootten R, Sommerville C (2007) The secondary structure of the unusually long 18S ribosomal RNA of the myxozoan Sphaerospora truttae and strutural evolutionary trends in the Myxozoa. Int J Parasitol 37:1281–1295

  • Jirků M, Bartošová P, Kodádková A, Mutschmann F (2011) Another Chloromyxid lineage: molecular phylogeny and redescription of Chloromyxum careni from the Asian horned frog Megophrys nasuta. J Eukaryot Microbiol 58(1):50–59

    Article  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 (1993) Scanning electron microscopic revision of common species of the genus Chloromyxum (Myxozoa: Myxosporea) infecting European freshwater fishes. Folia Parasitol 40:161–174

    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 

  • Morsy K, Abdel-Ghaffar F, Bashtar A-R, Mehlhorn H, Al Quraishy S, Abdel-Gaber R (2012) Morphology and small subunit ribosomal DNA sequence of Henneguya suprabranchiae (Myxozoa), a parasite of the catfish Clarias gariepinus (Clariidae) from the River Nile, Egypt. Parasitol Res 111:1423–1435

    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 

  • Rocha S, Graca C, Al-Quraishy S, Azevedo C (2013) Morphological and molecular characterization of a new myxozoan species (Myxosporea) infecting the gall bladder of Raja clavata (Chondrichthyes), from the Portuguese Atlantic coast. J Parasitol 99:307–317

    Article  CAS  PubMed  Google Scholar 

  • Rocha S, Graca C, Al-Quraishy S, Azevedo C (2014) Morphological and ultrastructural redescription of Chloromyxum leydigi Mingazzini, 1890 (Myxozoa: Myxosporea), type species of the genus, infecting the gall bladder of the marine cartilaginous fish Torpedo marmorata Risso (Chondrichthyes: Torpedinidae), from the Portuguese Atlantic coast. Folia Parasitol 61:1–10

    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 

  • Sanders JL, Jaramillo AG, Ashford JE, Feist SW, Lafferty KD, Kent ML (2015) Two myxozoans from the urinary tract of Topsmelt, Atherinops affinis. J Parasitol 101(5):577–586

    Article  PubMed  Google Scholar 

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

    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 25:4876–4882

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tinsley RC, Tinsley MC (2016) Tracing ancient evolutionary divergence in parasites. Parasitology 143:1902–1916

    Article  PubMed  Google Scholar 

  • Whipps CM, Adlard RD, Bryant MS, Lester RJG, Findlay 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 sp.n. from sweeper (Pempheris ypsilychnus). J Eukuryot Microbiol 50:215–219

    Article  Google Scholar 

  • Zhang JY, Zhao YL, Batueva MD, Luo D, Xing ZF, Zhang QQ, Liu XH (2017) Redescription of Chloromyxum ellipticum Li & Nie, 1973 (Myxosporea: Chloromyxidae) infecting the gall bladder of grass carp Ctenpharyngodon idellus Valenciennes, 1844, supplemented by morphological and molecular characteristics. Parasitol Res 116:1479–1486

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The present work was financially supported by the Natural Sciences Foundation of China (31472296) and Russian Fund 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., Voronin, V.N., Dudin, A.S. et al. Morphological and molecular characterization of a new cyprinid gall bladder-infecting Chloromyxum species, Chloromyxum peleci sp. n. (Myxozoa: Chloromyxidae), from Pelecus cultratus (L.) in Russia. Parasitol Res 116, 2239–2248 (2017). https://doi.org/10.1007/s00436-017-5527-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-017-5527-6

Keywords