Parasitology Research

, Volume 113, Issue 7, pp 2515–2524 | Cite as

First report of Kudoa species in the somatic muscle of the Japanese parrotfish Calotomus japonicus (Scaridae) and a description of Kudoa igami, n. sp. (Myxozoa: Multivalvulida)

  • Sho Shirakashi
  • Koji Yamane
  • Hiroe Ishitani
  • Tetsuya Yanagida
  • Hiroshi Yokoyama
Original Paper

Abstract

Three species of the Kudoid parasite (Myxozoa: Multivalvulida) were observed in the somatic muscle of Japanese parrotfish Calotomus japonicus caught off the coast of western Japan. All three species formed pseudocysts in myofibers and caused subclinical infections. The three Kudoa species were distinguished by spore morphology, as well as their 18S and 28S rDNA sequences. We identified a previously undescribed taxa Kudoa igami n. sp. with spores that were stellate with rounded peripheral edges and five to six polar capsules (prevalence 29.3 %). Kudoa igami n. sp. were morphologically most similar to Kudoa neothunni but were distinguishable by a more rounded shape in the apical view. Molecular analyses demonstrated that the K. igami n. sp. is closely related to Kudoa thalassomi; however, the similarity in the 28S rDNA sequence was <96 % and the spore morphology was different. We found Kudoa thalassomi in one sample (prevalence 2.4 %), which is a new host and geographical record for this species. Kudoa lateolabracis, which causes postmortem myoliquefaction in Chinese sea bass Lateolabrax sp. and olive flounder Paralichthys olivaceus was found in Japanese parrotfish (prevalence 41.5 %) for the first time, but did not cause myoliquefaction. We also expanded the host record for the brain-infecting Kudoa yasunagai (prevalence 94.1 %). In addition, an unidentified microsporidia was observed in the somatic muscle (prevalence 23.3 %).

Keywords

Kudoa igami Calatomus japonicas Pseudocyst Kudoa thalassomi Kudoa lateolabracis Kudoa yasunagai 

References

  1. Adlard RD, Bryant MS, Whipps CM, Kent ML (2005) Multivalvulid myxozoans from eastern Australia: three new species of Kudoa from scombrid and labrid fishes of the Great Barrier Reef, Queensland, Australia. J Parasitol 91(5):1138–1142PubMedCrossRefGoogle Scholar
  2. Arai Y, Matsumoto K (1953) On a new sporozoa, Hexacapsula neothunni gen. et sp. nov., from the muscle of yellowfin tuna, Neothunnus macropterus. Bull Jap Soc Sci Fish 18:293–299Google Scholar
  3. Burger MAA, Adlard RD (2010) Phenotypic variation in a significant spore character in Kudoa (Myxosporea: Multivalvulida) species infecting brain tissue. Parasitology 137(12):1759–1772PubMedCrossRefGoogle Scholar
  4. Burger MAA, Adlard RD (2011) Low host specificity in the Kudoidae (Myxosporea: Multivalvulida) including seventeen new host records for Kudoa thalassomi. Folia Parasitol 58(1):1–16PubMedCrossRefGoogle Scholar
  5. Fiala I (2006) The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. Int J Parasitol 36(14):1521–1534PubMedCrossRefGoogle Scholar
  6. Heiniger H, Adlard RD (2012) Host specificity and local infection dynamics of Kudoa leptacanthae n. sp (Multivalvulida: Kudoidae) from the pericardial cavity of two Zoramia spp. (Perciformes: Apogonidae) at Lizard Island lagoon, Queensland, Australia. Parasitol Int 61(4):697–706PubMedCrossRefGoogle Scholar
  7. Heiniger H, Cribb TH, Adlard RD (2013) Intra-specific variation of Kudoa spp. (Myxosporea: Multivalvulida) from apogonid fishes (Perciformes), including the description of two new species, K. cheilodipteri n. sp and K. cookii n. sp., from Australian waters. Syst Parasitol 84(3):193–215PubMedCrossRefGoogle Scholar
  8. Hillis DM, Dixon MT (1991) Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol 66(4):411–453PubMedCrossRefGoogle Scholar
  9. Huelsenbeck JP, Ronquist F (2001) MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17(8):754–755PubMedCrossRefGoogle Scholar
  10. Iwashita Y et al (2013) Food poisoning associated with Kudoa septempunctata. J Emerg Med 44(5):943–945PubMedCrossRefGoogle Scholar
  11. Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30(4):772–780PubMedCentralPubMedCrossRefGoogle Scholar
  12. Kawai T et al (2012) Identification of Kudoa septempunctata as the causative agent of novel food poisoning outbreaks in Japan by consumption of Paralichthys olivaceus in raw fish. Clin Infect Dis 54(8):1046–1052PubMedCrossRefGoogle Scholar
  13. Kent ML et al (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48(4):395–413PubMedCrossRefGoogle Scholar
  14. Li YC, Sato H, Tanaka S, Ohnishi T, Kamata Y, Sugita-Konishi Y (2013) Characterization of the ribosomal RNA gene of Kudoa neothunni (Myxosporea: Multivalvulida) in tunas (Thunnus spp.) and Kudoa scomberi n. sp in a chub mackerel (Scomber japonicus). Parasitol Res 112(5):1991–2003PubMedCrossRefGoogle Scholar
  15. Lom J, Dyková I (2006) Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol 53(1):1–36PubMedCrossRefGoogle Scholar
  16. Martinez de Velasco G, Rodero M, Cuellar C, Chivato T, Mateos JM, Laguna R (2008) Skin prick test of Kudoa sp. antigens in patients with gastrointestinal and/or allergic symptoms related to fish ingestion. Parasitol Res 103(3):713–715PubMedCrossRefGoogle Scholar
  17. Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y (2010) Kudoa septempunctata n. sp (Myxosporea: Multivalvulida) from an aquacultured olive flounder (Paralichthys olivaceus) imported from Korea. Parasitol Res 107(4):865–872PubMedCrossRefGoogle Scholar
  18. Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y (2011) Kudoa iwatai and two novel Kudoa spp., K. trachuri n. sp. and K. thunni n. sp. (Myxosporea: Multivalvulida), from daily consumed marine fish in western Japan. Parasitol Res 108(4):913–926PubMedCrossRefGoogle Scholar
  19. Miller TL, Adlard RD (2013) Unicapsula species (Myxosporea: Trilosporidae) of Australian marine fishes, including the description of Unicapsula andersenae n. sp. in five teleost families off Queensland, Australia. Parasitol Res 112(8):2945–2957PubMedCrossRefGoogle Scholar
  20. Moran JDW, Whitaker DJ, Kent ML (1999) A review of the myxosporean genus Kudoa Meglitsch, 1947, and its impact on the international aquaculture industry and commercial fisheries. Aquaculture 172(1–2):163–196CrossRefGoogle Scholar
  21. Nylander JAA (2004) MrModeltest v2. Program distributed by the author. Uppsala University, Evolutionary Biology CentreGoogle Scholar
  22. Patashnik M, Groninger HS Jr, Barnett H, Kudo G, Koury B (1982) Pacific Whiting, Merluccius productus. Abnormal muscle texture caused by myxosporidian-induced proteolysis. Mar Fish Rev 44:1–12Google Scholar
  23. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19(12):1572–1574PubMedCrossRefGoogle Scholar
  24. Sato H (2011) Biology of the myxozoa, a newly recognized parasitic pathogen causing food poisoning. Yamaguchi. J Vet Med 38:1–26Google Scholar
  25. Stamatakis A, Hoover P, Rougemont J (2008) A rapid bootstrap algorithm for the RAxML web servers. Syst Biol 57(5):758–771PubMedCrossRefGoogle Scholar
  26. Stehr C, Whitaker DJ (1969) Host–parasite interaction of the myxosporean Kudoa paniformis (Kabata & Whitaker 1981) and Kudoa thyrsites (Gilchrist 1924) in the muscle of the Pacific whiting, Merluccius productus (Ayres): an ultrastructural study. J Fish Dis 9:505–517CrossRefGoogle Scholar
  27. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony, version 4.0b10. Sinauer Associates, MassachusettsGoogle Scholar
  28. Whipps CM, Kent ML (2006) Phylogeography of the cosmopolitan marine parasite Kudoa thyrsites (Myxozoa: Myxosporea). J Eukaryot Microbiol 53(5):364–373PubMedCrossRefGoogle Scholar
  29. Whipps CM, Adlard RD, Bryant MS, Kent ML (2003a) Two unusual myxozoans, Kudoa quadricornis n. sp (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp (Multivalvulida) from the muscle of Spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. J Parasitol 89(1):168–173PubMedCrossRefGoogle Scholar
  30. Whipps CM, Adlard RD, Bryant MS, Lester RJ, Findlay V, Kent ML (2003b) First report of three Kudoa species from eastern Australia: Kudoa thyrsites from mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). J Eukaryot Microbiol 50(3):215–219PubMedCrossRefGoogle Scholar
  31. Whipps CM et al (2004) Phylogeny of the multivalvulidae (Myxozoa : Myxosporea) based on comparative ribosomal DNA sequence analysis. J Parasitol 90(3):618–622PubMedCrossRefGoogle Scholar
  32. Yokoyama H (2003) A review: gaps in our knowledge on myxozoan parasites of fishes. Fish Pathol 38(4):125–136CrossRefGoogle Scholar
  33. Yokoyama H, Itoh N (2005) Two multivalvulid myxozoans causing postmortem myoliquefaction: Kudoa megacapsula n. sp from red barracuda (Sphyraena pinguis) and Kudoa thyrsites from splendid alfonso (Beryx splendens). J Parasitol 91(5):1132–1137PubMedCrossRefGoogle Scholar
  34. Yokoyama H, Whipps CM, Kent ML, Mizuno K, Kawakami H (2004) Kudoa thyrsites from Japanese flounder and Kudoa lateolabracis n. sp from chinese sea bass: causative myxozoans of post-mortem myoliquefaction. Fish Pathol 39(2):79–85CrossRefGoogle Scholar
  35. Yokoyama H, Yanagida T, Takemaru I (2006) The first record of Kudoa megacapsula (Myxozoa : Multivalvulida) from farmed yellowtail Seriola quinqueradiata originating from wild seedlings in South Korea. Fish Pathol 41(4):159–163CrossRefGoogle Scholar
  36. Yokoyama H, Yanagida T, Shirakashi S (2012) Kudoa ogawai n. sp (Myxozoa: Multivalvulida) from the trunk muscle of Pacific barrelfish Hyperoglyphe japonica (Teleostei: Centrolophidae) in Japan. Parasitol Res 110(6):2247–2254PubMedCrossRefGoogle Scholar
  37. Yokoyama H, Suzuki J, Shirakashi S (2014) Kudoa hexapunctata n. sp. (Myxozoa: Multivalvulida) from the somatic muscle of Pacific bluefin tuna Thunnus orientalis and re-description of K. neothunni in yellowfin tuna T. albacares. Parasitol Int 63:571–579Google Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2014

Authors and Affiliations

  • Sho Shirakashi
    • 1
  • Koji Yamane
    • 2
  • Hiroe Ishitani
    • 1
  • Tetsuya Yanagida
    • 3
  • Hiroshi Yokoyama
    • 4
  1. 1.Fisheries LaboratoryKinki UniversityWakayamaJapan
  2. 2.Wakayama Prefectural Fisheries Experimental StationWakayamaJapan
  3. 3.Department of ParasitologyAsahikawa Medical UniversityAsahikawaJapan
  4. 4.Department of Aquatic Bioscience, Graduate School of Agricultural and Life SciencesUniversity of TokyoTokyoJapan

Personalised recommendations