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Acta Parasitologica

, Volume 64, Issue 2, pp 347–351 | Cite as

The Phylogenetic Position of Spironucleus sp. (Diplomonadida: Hexamitidae) from the Intestine of Chinese Sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae)

  • Natalia DenikinaEmail author
  • Ilya Kondratov
  • Natalia Belkova
  • Sergey Sokolov
Original Paper
  • 45 Downloads

Abstract

Introduction

The Chinese (Amur) sleeper (Perccottus glenii Dybowski, 1877) (Actinopterygii: Odontobutidae) is a freshwater fish species with high invasive potential. Diplomonads have been detected in the intestines of Chinese sleepers using light microscopy.

Aim

The aim of this study was to identify the diplomonads in Chinese sleepers using molecular-genetic methods.

Materials and methods

The fish used in this analysis were caught in the following bodies of water in Russia between 2014 and 2016: Lake Dolgoe, the floodplain of the Ingoda River (Amur River basin), the Tsna River (the Oka River basin), and the littoral of the Kotlin Island (Gulf of Finland). Partial sequences of small subunit rRNA genes were obtained for the intestinal diplomonads of Chinese sleeper.

Results

The analysis of all sequenced samples revealed the presence of Spironucleus salmonis Moore, 1922; other Spironucleus species were not found in the sampled fish. With 82% probability, the sampled sequences of diplomonads from Chinese sleeper formed a separate cluster in the clade of S. salmonis on the phylogenetic tree.

Conclusion

This is the first record of S. salmonis in fish in the family Odontobutidae.

Keywords

Perccottus glenii Spironucleus salmonis Molecular-genetic methods Small subunit rRNA gene Phylogenetic analysis 

Notes

Acknowledgements

The authors would like to thank Sergey Kirilchik for his help and support. The research was supported by the state orders 0345–2019–0002 (LIN SB RAS) and 0109–2014–0028 (IPEE RAS).

References

  1. 1.
    Antal L, Szekely C, Molnar K (2015) Parasitic infections of two invasive fish species, the Caucasian dwarf goby and the Amur sleeper, Hungary. Acta Vet Hung 63(4):472–484.  https://doi.org/10.1556/004.2015.044 CrossRefPubMedGoogle Scholar
  2. 2.
    Bel’kova NL, Dzyuba EV, Sukhanova EV (2008) Molecular-genetic detection of a nonpathogenic genotype of Spironucleus barkhanus (Diplomonadida: Hexamitidae) in the black baikal grayling (Thymallus arcticus baicalensis Dybowski, 1874). Biol Bull Russ Acad Sci 35(2):219–221CrossRefGoogle Scholar
  3. 3.
    Denikina N, Nebesnykh I, Maikova O, Dzyuba E, Belkova N (2016) Genetic diversity of Diplomonadida in fish of the genus Coregonus from south-eastern Siberia. Acta Parasitol 61(2):299–306.  https://doi.org/10.1515/ap-2016-0040 CrossRefPubMedGoogle Scholar
  4. 4.
    Denikina NN, Nebesnukh IA, Sukhanova EV, Belkova NL, Rusinek OT, Dzyuba EV (2011) Development and testing of detection representatives order Diplomonadida for investigation of fish infestation. Biol Sci Kaz 4:28–33 (In Russian) Google Scholar
  5. 5.
    Fard MRS, Jørgensen A, Sterud E, Bleiss W, Poynton SL (2007) Ultrastructure and molecular diagnosis of Spironucleus salmonis (Diplomonadida) from rainbow trout Oncorhynchus mykiss in Germany. Dis Aquat Organ 75:37–50.  https://doi.org/10.3354/dao075037 CrossRefPubMedGoogle Scholar
  6. 6.
    Fenchel T, Bernard C, Esteban G, Finlay BJ, Hansen PJ, Iversen N (1995) Microbial diversity and activity in a Danish Fjord with anoxic deep water. Ophelia 43(1):45–100.  https://doi.org/10.1080/00785326.1995.10430576 CrossRefGoogle Scholar
  7. 7.
    Guz L, Puk K (2015) First molecular identification of Spironucleus salmonis (Diplomonadida) from diseased rainbow trout Oncorchynchus mykiss in Poland. Med Weter 71(8):497–499Google Scholar
  8. 8.
    Hoffman G (1999) Parasites of north American freshwater fishes. Cornell University Press, Ithaca, p 539Google Scholar
  9. 9.
    Jørgensen A, Sterud D (2006) The marine pathogenic genotype of Spironucleus barkhanus from farmed salmonids redescribed as Spironucleus salmonicida n. sp. J Eukaryot Microbiol 53:531–541.  https://doi.org/10.1111/j.1550-7408.2006.00144.x CrossRefPubMedGoogle Scholar
  10. 10.
    Jørgensen A, Sterud E (2004) SSU rRNA gene sequence reveals two genotypes of Spironucleus barkhanus (Diplomonadida) from farmed and wild Arctic charr Salvelinus alpinus. Dis Aquat Organ 62:93–96.  https://doi.org/10.3354/dao062093 CrossRefPubMedGoogle Scholar
  11. 11.
    Jørgensen A, Torp K, Bjorland MA, Poppe TT (2011) Wild Arctic char Salvelinus alpinus and trout Salmo trutta: hosts and reservoir of the salmonid pathogen Spironucleus salmonicida (Diplomonadida; Hexamitidae). Dis Aquat Organ 97:57–63.  https://doi.org/10.3354/dao02404 CrossRefPubMedGoogle Scholar
  12. 12.
    Kimura M (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874.  https://doi.org/10.1093/molbev/msw054 CrossRefPubMedPubMedCentralGoogle Scholar
  14. 14.
    Meseck EK, French TW, Grimmett SG, Bartlett SL, Wooster GA, Getchell RG, Schachte JH Jr, Bowser PR (2007) Gross and microscopic pathology associated with large cavernous lesions in muscle of chinook salmon from Lake Ontario. J Wildl Dis 43:111–115.  https://doi.org/10.7589/0090-3558-43.1.111 CrossRefPubMedGoogle Scholar
  15. 15.
    Molnár K, Székely CS (1995) Parasitological survey of some important fish species of the Lake Balaton. Parasitol Hung 28:63–82Google Scholar
  16. 16.
    Nebesnykh IA, Denikina NN, Kondratov IG, Khanaev IV, Smolin IN, Belkova NL, Dzyuba EV (2017) First description of Enterocytozoonidae (Fungi: Microsporidia) in fish from lake Baikal. Int J Appl Fundam Res 10:86–89.  https://doi.org/10.17513/mjpfi.11866 CrossRefGoogle Scholar
  17. 17.
    Paull GC, Matthews RA (2001) Spironucleus vortens, a possible cause of holein-the-head disease in cichlids. Dis Aquat Organ 45:197–202.  https://doi.org/10.3354/dao045197 CrossRefPubMedGoogle Scholar
  18. 18.
    Poynton SL, Fard MRS, Jenkins J, Ferguson HW (2004) Ultrastructure of Spironucleus salmonis n. comb. (formerly Octomitus salmonis sensu Moore 1922, Davis 1926, and Hexamita salmonis sensu Ferguson 1979), with a guide to Spironucleus species. Dis Aquat Organ 60:49–64.  https://doi.org/10.3354/dao060049 CrossRefPubMedGoogle Scholar
  19. 19.
    Poynton SL, Sterud E (2002) Guidelines for species descriptions of diplomonad flagellates from fish. J Fish Dis 25:15–31.  https://doi.org/10.1046/j.1365-2761.2002.00331.x CrossRefGoogle Scholar
  20. 20.
    Pugachev ON (2001) Checklist of the freshwater fish parasites of the Northern Asia. St. Petersburg, Zoological Institute RAS, Sankt-Peterburg, p 242Google Scholar
  21. 21.
    Reshetnikov AN (2010) The current range of Amur sleeper Perccottus glenii Dybowski, 1877 (Odontobutidae, Pisces) in Eurasia. Russ J Biol Invasions 1:119–126.  https://doi.org/10.1134/S2075111710020116 CrossRefGoogle Scholar
  22. 22.
    Reshetnikov AN, Sokolov SG, Protasova EN (2017) Detection of a neglected introduction event of the invasive fish Perccottus glenii using parasitological analysis. Hydrobiologia 788:65–73.  https://doi.org/10.1007/s10750-016-2987-0 CrossRefGoogle Scholar
  23. 23.
    Roxstrom-Lindquist K, Jerlström-Hultqvist J, Jorgensen A, Troell K, Svärd SG, Andersson JO (2010) Large genomic differences between the morphologically indistinguishable diplomonads Spironucleus barkhanus and Spironucleus salmonicida. BMC Genom 11:1–14.  https://doi.org/10.1186/1471-2164-11-258 CrossRefGoogle Scholar
  24. 24.
    Sokolov SG, Lebedeva DI, Yadrenkina EN (2013) The first data on the parasite fauna of Amur sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) from waterbodies of forest-steppe zone of West Siberian plains. Parasitologiya 47(6):448–460 (In Russian) Google Scholar
  25. 25.
    Sokolov SG, Protasova EN (2014) Parasites of introduced rotan Perccottus glenii (Actinopterygii: Odontobutidae) at the northern border of host range. Russ J Biol Invasions 3:83–87 (In Russian) Google Scholar
  26. 26.
    Sokolov SG, Protasova EN, Lebedeva DI, Gorlacheva EP, Gorlachev VP (2016) Parasites of the Amur sleeper Perccottus glenii Dybowski, 1877 (Actinopterygii: Odontobutidae) in waterbodies of upper Amur. Parasitologiya 50(1):69–81 (In Russian) Google Scholar
  27. 27.
    Sterud E (1998) Electron microscopical identification of the flagellate Spironucleus torosa (Hexamitidae) from burbot Lota lota (Gadidae) with comments upon its probable introduction to this freshwater host. J Parasitol 84:947–953CrossRefPubMedGoogle Scholar
  28. 28.
    Sterud E (1998) Ultrastructure of Spironucleus torosa Poynton & Morrison, 1990 (Diplomonadida: Hexamitidae), in cod Gadus morhua (L.) and saithe Pollachius virens (L.) from south-eastern Norway. Eur J Protistol 34:69–77CrossRefGoogle Scholar
  29. 29.
    Sterud E, Mo TA, Poppe TT (1998) Systemic spironucleosis in sea-farmed Atlantic salmon Salmo salar, caused by Spironucleus barkhanus transmitted from feral Arctic char Salvelinus alpinus? Dis Aquat Organ 33:63–66.  https://doi.org/10.3354/dao033063 CrossRefPubMedGoogle Scholar
  30. 30.
    Williams CF, Lloyd D, Poynton SL, Jorgensen A, Millet COM, Cable J (2011) Spironucleus species: economically important fish pathogens and enigmatic single-celled eukaryotes. J Aquac Res Dev 2:13.  https://doi.org/10.4172/2155-9546S2-002 CrossRefGoogle Scholar
  31. 31.
    Xiao WH, Wang JG (2000) Phylogeny of Hexamita parasitic in Xenocyprinae based on cladistic analysis of morphological characteristics with consideration of coevolution between hosts and host-parasites. Acta Hydrobiol Sin 24:122–127Google Scholar
  32. 32.
    Zolovs M, Priekule M, Kārkliņš A, Kirjušina M (2016) New records of parasite fauna in Perccottus glenii Dybowski, 1877 from lakes of Latgale region (Latvia). In: Abstracts of the 58 international scientific conference of Daugavpils University. Daugavpils Universitātes Akadēmiskais apgāds “Saule”, Daugavpils. pp 93–94Google Scholar

Copyright information

© Witold Stefański Institute of Parasitology, Polish Academy of Sciences 2019

Authors and Affiliations

  • Natalia Denikina
    • 1
    Email author
  • Ilya Kondratov
    • 1
  • Natalia Belkova
    • 1
  • Sergey Sokolov
    • 2
  1. 1.Limnological Institute Siberian Branch of the Russian Academy of SciencesIrkutskRussia
  2. 2.Severtsov Institute of Ecology and Evolution RASMoscowRussia

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