Pseudokabatana alburnus n. gen. n. sp., (Microsporidia) from the liver of topmouth culter Culter alburnus (Actinopterygii, Cyprinidae) from China

  • X. H. Liu
  • G. D. Stentiford
  • V. N. Voronin
  • H. Sato
  • A. H. Li
  • J. Y. ZhangEmail author
Fish Parasitology - Review


We describe the type species of a novel genus of microsporidian parasite, Pseudokabatana alburnus n. gen. n. sp., infecting the liver of topmouth culter, Culter alburnus Basilewsky, 1855, from Lake Poyang off Xingzi county, Jiangxi Province, China. The parasite elicits formation of spherical xenomas of up to 1.2 mm in diameter containing all observed life stages from early merogonal plasmodia to mature spores contained within the cytoplasm of host hepatocytes. Merogonal plasmodia existed in direct contact with the host cytoplasm and contained up to 20 visible nuclei. Plasmotomy of the multinucleate plasmodium led to formation of uninucleate cells in which the nucleus underwent further division to form bi-nucleate presporonts, sporonts (defined by cells with a thickened endospore) and eventually sporoblasts (containing pre-cursors of the spore extrusion apparatus). Mature spores were pyriform and monokaryotic, measuring 2.3 ± 0.19 μm long and 1.3 ± 0.10 μm wide. Spores possessed a bipartite polaroplast and 5–6 coils of a polar filament, in a single rank. The obtained partial SSU rRNA gene sequence, 1383 bp in length, did not match any of microsporidia available in GenBank. SSU rDNA-based phylogenetic analysis indicated a new taxon branching with Kabatana rondoni, a parasite infecting the skeletal muscle of Gymnorhamphichthys rondoni from the Amazon River. Due to different host and tissue tropism, the novel taxon did not fit the diagnostic criteria for the genus Kabatana. Further, based on SSU rDNA-inferred phylogenetic analyses, different ultrastructural features of developmental stages, and ecological considerations, a new genus Pseudokabatana and type species Pseudokabatana alburnus n. sp. was erected for the parasite in topmouth culter.


Kabatana Pseudokabatana alburnus n. gen. n. sp. Ultrastructure Xenoma 



The authors are much indebted to Yuliya Y. Sokolova (Department of Comparative Biological Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge LA, USA and Institute of Cytology, Russian Academy of Sciences, Russia) and Tokarev YS and Issi IV (All-Russian Institute of Plant Protection, Russian Academy of Agriculture Sciences, Russia) for their help to discern the ultrastructural characters.

Funding information

The study was financially supported by Natural Science Foundation of China (31772411) and Free-Orientation project of Institute of Hydrobiology, Chinese Academy of Sciences. GDS was supported by the UK department for Environment, Food and Rural Affairs (Defra) under contract FB002.


  1. Abdel-Ghaffar F, Bashtar AR, Morsy K, Mehlhorn H, Quraishy SA, Al-Rasheid K, Abdel-Geber R (2012) Morphological and molecular biological characterization of Pleistophora aegytiaca sp. nov. infecting the Red Sea fish Saurida tumbil. Parasitol Res 110:741–752CrossRefGoogle Scholar
  2. Aranguren LF, Han JE, Tang FJ (2017) Enterocytozoon hepatopenaei (EHP) is a risk factor for acute hepatopancreatic necrosis disease (AHPND) and septic hepatopancreatic necrosis (SHPN) in the Pacific shrimp Penaeus vannamei. Aquaculture 471:37–42CrossRefGoogle Scholar
  3. Bell AS, Aoki T, Yokoyama H (2001) Phylogenetic relationships among Microsporidia based on rDNA sequence data, with particular reference to fish-infecting Microsporidium Balbiani 1884 species. J Eukaryot Microbiol 48:258–265CrossRefGoogle Scholar
  4. Cao WX (2011) The current situation and protection strategies of fish resources in Yangtze River. Jiangxi Fish Sci Technol 2:1–4 (In Chinese)Google Scholar
  5. Casal G, Matos E, Teles-Grilo L, Azevedo C (2010) Ultrastructural and molecular characterization of a new microsporidium parasite from the Amazonian fish, Gymnorhamphichthys rondoni (Rhamphichthyidae). J Parasitol 96:1155–1163CrossRefGoogle Scholar
  6. Casal G, Matos E, Garcia P, Al-Quraishy S, Azevedo C (2012) Ultrastructural and molecular studies of Microgemma carolinus n. sp. (Microsporidia), a parasite of the fish Trachinotus carolinus (Carangidae) in Southern Brazil. Parasitology 139:1720–1728CrossRefGoogle Scholar
  7. Casal G, Rocha S, Costa G, Al-Quraishy S, Azevedo C (2016) Ultrastructural and molecular characterization of Glugea serranus n. sp., a microsporidian infecting the black tail comber, Serranus atricauda (Teleostei: Serranidae), in the Madeira archipelago (Portugal). Parasitol Res 115:3963–3972CrossRefGoogle Scholar
  8. Chen QL (1955) The protozoan parasites from four species of Chinese pond fishes: Ctenopharyngodon idellus, Mylopharyngodon piceus, Aristichthys nobillis and Hypophthalmichthys molithrix I: the protozoan parasites of Ctenopharyngodon idellus. Acta Hydrobiol Sin 1:123–164 (In Chinese)Google Scholar
  9. Chen QL (1956a) The protozoan parasites from four species of Chinese pond fishes: Ctenopharyngodon idellus, Mylopharyngodon piceus, Aristichthys nobillis and Hypophthalmichthys molithrix II. The protozoan parasites of Mylopharyngodon piceus. Acta Hydrobiol Sin 1:19–42 (In Chinese)Google Scholar
  10. Chen QL (1956b) The protozoan parasites from four species of Chinese pond fishes: Ctenopharyngodon idellus, Mylopharyngodon piceus, Aristichthys nobillis and Hypophthalmichthys molithrix III. The protozoan parasites of Aristichthys nobillis and Hypophthalmichthys molithrix. Acta Hydrobiol Sin 2:279–298 (In Chinese)Google Scholar
  11. Chen QL, Xie XR (1960) Studies on Sporozoa from the freshwater fishes Ophicephalus maculatus and O. argus of China. Acta Hydrobiol Sin 2:171–196 (In Chinese)Google Scholar
  12. Fang CL, Chen WJ, Zhou HM, Zhang YP, Fu PF, He G, Wu B, Wang S (2016) The fish resources and their utilization in Lake Poyang. Jiangsu Agri Sci 44:233–243 (In Chinese)Google Scholar
  13. 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 59:307–321CrossRefGoogle Scholar
  14. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp Ser 41:95–98Google Scholar
  15. He XJ (1988) A preliminary study on Thelohaniasis of Penaeus penlicillatus. J Tropi Oceanol 1:102–106 (In Chinese)Google Scholar
  16. He XJ, Li ZF (1985) Pleistophora pseudorasborae, a new species of Microsporidia (Sporozoa: Myxosporidia). Acta Zootaxon Sin 10:234–238 (In Chinese)Google Scholar
  17. Kent ML, Shaw RW, Sanders JL (2014) Microsporidia in fish. 2014. In: Weiss LM, Becnel JJ (eds) Microsporidia: pathogens of opportunity, 1st edn. Wiley Blackwell, Oxford, pp 493–520Google Scholar
  18. Lom J, Nilsen F (2003) Fish microsporidia: fine structural diversity and phylogeny. Int J Parasitol 33:107–127CrossRefGoogle Scholar
  19. Lom J, Dyková I, Shaharom F (1990) Microsporidium arthuri n. sp., parasite of Pangasius sutchi (Pangasiidae, Siluroidea) in South-east Asia. Dis Aquat Org 8:65–67CrossRefGoogle Scholar
  20. Lom J, Dykova I, Tonguthai K (1999) Kabataia gen. n., a new genus proposed for Microsporidium spp. infecting trunk muscles of fishes. Dis Aquat Org 38:39–46CrossRefGoogle Scholar
  21. Lom J, Nilsen F, Urawa S (2001) Redescription of Microsporidium takedai (Awakura, 1974) as Kabatana takedai (Awakura, 1974) comb. n. Dis Aquat Org 44:223–230CrossRefGoogle Scholar
  22. McGourty KR, Kinziger AP, Hendrickson GL, Goldsmith GH, Casal G, Azevedo C (2007) A new microsporidian infecting the musculature of the endangered tidewater goby (Gobiidae). J Parasitol 93:655–660CrossRefGoogle Scholar
  23. Nilsen F (2000) Small subunit ribosomal DNA phylogeny of microsporidia with particular reference to genera that infect fish. J Parasitol 86:128–133CrossRefGoogle Scholar
  24. Page RD (1996) TreeView: an application to display phylogenetic trees on personal computers. Comput Appl Biosci 12:357–358Google Scholar
  25. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256CrossRefGoogle Scholar
  26. Ralphs JR, Matthews RA (1986) Hepatic microsporidiosis of juvenile grey mullet, Chelon labrosus(Risso) due to Microgemma hepaticus gen. nov. sp. nov. J Fish Dis 9:225–242CrossRefGoogle Scholar
  27. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574CrossRefGoogle Scholar
  28. Simakova A, Tokarev YS, Issi IV (2018) A new microsporidium Fibrilla daphinae g. n. sp. n. infecting Daphnia magna (Crustacea: Cladocera) in Siberia and its taxonomic placing within a new family Fibrillasporidae and new superfamily Tubulinosematidea (Opisthosporidia: Microsporidia). Parasitol Res 117:759–766CrossRefGoogle Scholar
  29. Stentiford GD, Feist SW, Stone DM, Bateman KS, Dunn AM (2013a) Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends Parasitol 29:567–578CrossRefGoogle Scholar
  30. Stentiford GD, Bateman KS, Feist SW, Chambers E, Stone DM (2013b) Plastic parasites: extreme dimorphism creates a taxonomic conundrum in the phylum Microsporidia. Int J Parasitol 43:339–352CrossRefGoogle Scholar
  31. Stentiford GD, Becnel JJ, Weiss LM, Keeling PJ, Dider ES, Willams BAP, Bjornson S, Kent ML, Freeman MA, Brown MJF, Troemel ER, Roesel K, Sokolova Y, Snowden KF, Solter L (2015) Microsporidia: emergent pathogens in the global food chain. Trends Parasitol 32:336–348CrossRefGoogle Scholar
  32. Stentiford GD, Ross S, Minardi D, Feist SW, Bateman KS, Gainey PA, Troman C, Bass D (2018) Evidence for trophic transfer of Indosporus octospora and Ovipleistophora arlo n. sp. (Microsporidia) between crustacean and fish hosts. Parasitology 145:1105–1117CrossRefGoogle Scholar
  33. Su YL, Feng J, Sun XX, Jiang JZ, Guo ZX, Ye LT, Xu LW (2014) A new species of Glugea Thelohan, 1891 in the red sea bream Pagrus major (Temminck & Schlegel) (Teleostei: Sparidae) from China. Syst Parasitol 89:175–183CrossRefGoogle Scholar
  34. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729CrossRefGoogle Scholar
  35. 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 25:4876–4883CrossRefGoogle Scholar
  36. Tourtip S, Wongtripop S, Stentiford GD, Bateman KS, Sriurairarana S, Chavadej J, Sritunyalucksana K, Withyachumnarnkul B (2009) Enterocytozoon hepatopenaei sp. nov. (Microsporidia: Enterocytozoonidae) a parasite of the black tiger shrimp Penaeus monodon (Decapoda: Penaeidae) fine structure and phylogenetic relationships. J Invertebr Pathol 102:21–29CrossRefGoogle Scholar
  37. Vossbrinck CR, Debrunner-Vossbrinck BA (2005) Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitol 52:131–142CrossRefGoogle Scholar
  38. Wang Y, Li XC, Fu GH, Zhao S, Chen YG, Wang H, Chen TT, Zhou JF, Fang WF (2017) Morphology and phylogeny of Ameson portunus n. sp. (Microsporidia) infecting the swimming crab Portunus trituberculatus from China. Eur J Protistol 61:122–136CrossRefGoogle Scholar
  39. Willams BA, Hamilton KM, Jones MD, Bass D (2018) Group-specific environmental sequencing reveals high levels of ecological heterogenity across the mcirosporidian radiation. Env Microbiol Rep 10:328–336CrossRefGoogle Scholar
  40. Wu HB, Wu YS, Wu ZH (2005) Occurence of a new Microspordium in the abdominal cavity of Epinephelus akaara. Acta Hydrobiol Sin 29:150–154 (In Chinese)Google Scholar
  41. Xu LW, Liu XH, Zhang JY, Liu GF, Feng J (2017) Outbreak of enteric microsporidiosis of hatchery-bred juvenile groupers, Epinephelus spp., associated with a new intranuclear microporidian in China. J Fish Dis 40:183–189CrossRefGoogle Scholar
  42. Yan YY, Liu XH, Xu LW, Zhang JY (2018) The taxonomic position of causative agent of enteric microsporidiosis of hatchery-bred juvenile grouper, Epinephelus spp., cultured in the area off coast of South China Sea. Acta Hydrobiol Sin 42:947–953 (In Chinese)Google Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Key Laboratory of Aquaculture Diseases Control, Ministry of Agriculture, State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of HydrobiologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.International Centre of Excellence for Aquatic Animal HealthCefas Weymouth LaboratoryDorsetUK
  4. 4.Centre for Sustainable Aquaculture Futures, College of Life and Environmental Sciences, Geoffrey PopeUniversity of ExeterExeterUK
  5. 5.Berg State Research Institute on Lake and River FisheriesSt. PetersburgRussia
  6. 6.Laboratory of Parasitology, Joint Faculty of Veterinary MedicineYamaguchi UniversityYamaguchiJapan

Personalised recommendations