DOI QR코드

DOI QR Code

Molecular detection of Kudoa septempunctata (Myxozoa: Multivalvulida) in sea water and marine invertebrates

  • Paari, Alagesan (Department of Marine Bioscience, Gangneung-Wonju National University) ;
  • Jeon, Chan-Hyeok (Department of Marine Bioscience, Gangneung-Wonju National University) ;
  • Choi, Hye-Sung (Pathology Division, National Institute of Fisheries Science (NIFS)) ;
  • Jung, Sung-Hee (Pathology Division, National Institute of Fisheries Science (NIFS)) ;
  • Kim, Jeong-Ho (Department of Marine Bioscience, Gangneung-Wonju National University)
  • 투고 : 2017.05.08
  • 심사 : 2017.07.20
  • 발행 : 2017.08.31

초록

The exportation of cultured olive flounder (Paralichthys olivaceus) in Korea has been recently decreasing due to the infections with a myxozoan parasite Kudoa septempunctata, and there is a strong demand for strict food safety management because the food poisoning associated with consumption of raw olive flounder harbouring K. septempunctata has been frequently reported in Japan. The life cycle and infection dynamics of K. septempunctata in aquatic environment are currently unknown, which hamper establishment of effective control methods. We investigated sea water and marine invertebrates collected from olive flounder farms for detecting K. septempunctata by DNA-based analysis, to elucidate infection dynamics of K. septempunctata in aquaculture farms. In addition, live marine polychaetes were collected and maintained in well plates to find any possible actinosporean state of K. septempunctata. The level of K. septempunctata DNA in rearing water fluctuated during the sampling period but the DNA was not detected in summer (June-July in farm A and August in farm B). K. septempunctata DNA was also detected in the polychaetes Naineris laevigata intestinal samples, showing decreased pattern of 40 to 0%. No actinosporean stage of K. septempunctata was observed in the polychaetes by microscopy. The absence of K. septempunctata DNA in rearing water of fish farm and the polychaetes N. laevigata intestinal samples during late spring and early summer indicate that the infection may not occur during this period. N. laevigata was suspected as the possible alternate invertebrate host of K. septempunctata, but the actinosporean stage was not found by well plate method and further studies will be necessary. This research provides important baseline information for understanding the infection dynamics of K. septempunctata in olive flounder farms and further establishment of control strategies.

키워드

참고문헌

  1. Abdel-Baki AA, Mansour L, Al-Qahtani HA, Al-Omar SY, Al-Quraishy S. Morphology, seasonality and phylogenetic relationships of Ceratomyxa husseini n. sp. from the gall-bladder of Cephalopholis hemistiktos (Ruppell) (Perciformes: Serranidae) in the Arabian Gulf of Saudi Arabia. Syst Parasitol. 2015;91:91-9. https://doi.org/10.1007/s11230-015-9554-3
  2. Alama-Bermejo G, Sima R, Raga JA, Holzer AS. Understanding myxozoan infection dynamics in the sea: seasonality and transmission of Ceratomyxa puntazzi. Int J Parasitol. 2013;43:771-80. https://doi.org/10.1016/j.ijpara.2013.05.003
  3. Al-Qahtani HA, Mansour L, Al-Quraishy S, Abdel-Baki AS. Morphology, phylogeny and seasonal prevalence of Ceratomyxa arabica n. sp. (Myxozoa: Myxosporea) infecting the gallbladder of Acanthopagrus bifasciatus (Pisces: Sparidae) from the Arabian Gulf, Saudi Arabia. Parasitol Res. 2015;114:465-671. https://doi.org/10.1007/s00436-014-4204-2
  4. Canning EU, Okamura B. Biodiversity and evolution of the myxozoa. Adv Parasitol. 2003;56:43-131.
  5. Cobcroft JM, Battaglene SC. Ultraviolet irradiation is an effective alternative to ozonation as a sea water treatment to prevent Kudoa neurophila (Myxozoa: Myxosporea) infection of striped trumpeter Latris lineata (Forster). J Fish Dis. 2013;36:57-65. https://doi.org/10.1111/j.1365-2761.2012.01413.x
  6. Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R. DNA primers for amplification of mitochondrial cytochrome C oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol. 1994;3:294-9.
  7. Grabner DS, Yokoyama H, Shirakashi S, Kinami R. Diagnostic PCR assays to detect and differentiate Kudoa septempunctata, K. thyrsites and K. lateolabracis (Myxozoa, Multivalvulida) in muscle tissue of olive flounder (Paralichthys olivaceus). Aquaculture. 2012;338:36-40.
  8. Hallet SL, Bartholomew JL. Development and application of a duplex qPCR for river water samples to monitor the myxozoan parasite Parvicapsula minibicornis. Dis Aquat Org. 2009;86:36-50.
  9. Hallet SL, Bartholomew JL. Effects of water flow on the infection dynamics of Myxobolus cerebralis. Parasitology. 2007;135:371-84.
  10. Hallett SL, Ray RA, Hurst CN, Buckles GR, Atkinson SD, Bartholomew JL. Density of the waterborne parasite Ceratomyxa shasta and its biological effects on salmon. Appl Environ Microbiol. 2012;78:3724-31. https://doi.org/10.1128/AEM.07801-11
  11. Harada T, Kawai T, Jinnai M, Ohnishi T, Sugita-Konishi Y, Kumeda Y. Detection of Kudoa septempunctata 18S ribosomal DNA in patient fecal samples from novel food-borne outbreaks caused by consumption of raw olive flounder (Paralichthy solivaceus). J Clin Microbiol. 2012;50:2964-8. https://doi.org/10.1128/JCM.01218-12
  12. Hoz Franco E, Budy P. Linking environmental heterogeneity to the distribution and prevalence of Myxobolus cerebralis: a comparison across sites in a Northern Utah water shed. Trans Am Fish Soc. 2004;133:1176-89. https://doi.org/10.1577/T03-167.1
  13. Ishimaru K, Matsuura T, Tsunemoto K, Shirakashi S. Seasonal monitoring of Kudoa yasunagai from sea water and aquaculture water using quantitative PCR. Dis Aquat Org. 2014;108:45-52. https://doi.org/10.3354/dao02702
  14. Iwashita Y, Kamijo Y, Nakahashi S, Shindo A, Yokoyama K, Yamamoto A, Omori Y, Ishikura K, Fujioka M, Hatada T, Takeda T, Maruyama K, Imai H. Food poisoning associated with Kudoa septempunctata. J. Emerg. Med. 2013; 44:943-945.
  15. Karlsbakk E, Koie M. The marine myxosporean Sigmomyxa sphaerica (Thelohan, 1895) gen. n., comb. n. (syn. Myxidium sphaericum) from garfish (Belone belone (L.)) uses the polychaete Nereis pelagica L. as invertebrate host. Parasitol. Res. 2012;110:211-218. https://doi.org/10.1007/s00436-011-2471-8
  16. Kawai T, Sekizuka T, Yahata Y, Kuroda M, Kumeda Y, Iijima Y, Kamata Y, Sugita-Konishi Y, Ohnishi T. 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. 2012;54:1046-1052. https://doi.org/10.1093/cid/cir1040
  17. Kerans BL, Zale AV. The ecology of Myxobolus cerebralis. In Whirling Disease: Reviews and Current Topics (ed. Bartholomew, J. L. and Wilson, J. C.). American Fisheries Society Symposium. 29, Bethesda, Maryland, USA. 2002. p.145-166.
  18. Koie M. Spirorchid and serpulid polychaetes are candidates as invertebrate hosts for Myxozoa. Folia Parasitol. 2002;49:160-162 https://doi.org/10.14411/fp.2002.028
  19. Koie M. Whipps CM, Kent ML. Ellipsomyxa gobii (Myxozoa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelida: Polychaeta) as invertebrate hosts. Folia Parasitol. 2004;51:14-18. https://doi.org/10.14411/fp.2004.002
  20. Koie M, Karlsbakk E, Nylund A. A new genus Gadimyxa with three new species (Myxozoa, Parvicapsulidae) parasitic in marine fish (Gadidae) and the two host life cycle of Gadimyxa atlantica n. sp. J. Parasitol. 2007;93:1459-1467 https://doi.org/10.1645/GE-1256.1
  21. Koie M, Karlsbakk E, Nylund A. The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitol. 2008;55:100-104. https://doi.org/10.14411/fp.2008.013
  22. Koie M, Karlsbakk E, Einen ACB, Nylund A. A parvicapsulid (Myxozoa) infecting Sprattus sprattus and Clupea harengus (Clupeidae) in the Northeast Atlantic uses Hydroides norvegicus (Serpulidae) as invertebrate host. Folia Parasitol. 2013;60:149-154. https://doi.org/10.14411/fp.2013.016
  23. Lom J, Dykova I. Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitol. 2006;53:1-36. https://doi.org/10.14411/fp.2006.001
  24. Markussen T, Agusti C, Karlsbakk E, Nylund A, Brevik O, Hansen H. Detection of the myxosporean parasite Parvicapsula pseudobranchicola in Atlantic salmon (Salmo salar L.) using in situ hybridization (ISH). Parasite Vectors. 2015;8:1-6. https://doi.org/10.1186/s13071-014-0608-1
  25. Matsukane Y, Sato H, Tanaka S, Kamata Y, Sugita-Konishi Y. Kudoa septempunctata n. sp. (Myxosporea: Multivalvulida) from an aquacultured olive flounder (Paralichthys olivaceus) imported from Korea. Parasitol. Res. 2010;107:865-872. https://doi.org/10.1007/s00436-010-1941-8
  26. Maturana CS, Moreno RA, Labra FA, Gonzalez CA, Rozbaczylo N, Carrasco FD, Poulin E, DNA barcoding of marine polychaetes species of southern Patagonian fjords. Rev. Biol. Mar. Oceanogr. 2011;46:35-42. https://doi.org/10.4067/S0718-19572011000100005
  27. Miller TL, Adlard RD. Brain infecting kudoids of Australia's coral reefs, including a description of Kudoa lemniscati n. sp (Myxosporea: Kudoidae) from Lutjanus lemniscatus (Perciformes: Lutjanidae) off Ningaloo Reef, Western Australia. Parasitol. Int. 2012;61:333-342. https://doi.org/10.1016/j.parint.2012.01.002
  28. Nehring RB, Thompson KG, Taurman K, Atkinson W. Efficacy of passive sand filtration in reducing exposure of salmonids to the actinospore of Myxobolus cerebralis. Dis. Aquat. Org. 2003;57:77-83. https://doi.org/10.3354/dao057077
  29. Ray RA, Holt RA, Bartholomew JL. Relationship between temperature and Ceratomyxa shasta induced mortality in Klamath river salmonids. J. Parasitol. 2012;95:561-569.
  30. Rangel LF, Santos MJ, Cech G, Szekely C. Morphology, Molecular Data, and Development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate Host, Nereis diversicolor. J. Parasitol. 2009;95:561-569. https://doi.org/10.1645/GE-1777.1
  31. Rangel LF, Cech G, Szekely C, Santos MJ. A new actinospore type Unicapsulactinomyxon (Myxozoa), infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro Estuary (Portugal). Parasitology 2011; 138:698-712. https://doi.org/10.1017/S0031182011000163
  32. Rangel LF, Rocha S, Castro R, Severino R, Casal G, Azevedo C, Cavaleiro F, Santos MJ. The life cycle of Ortholinea auratae (Myxozoa: Ortholineidae) involves an actinospore of the triactinomyxon morphotype infecting a marine oligochaete. Parasitol. Res. 2015;114: 2671-2678. https://doi.org/10.1007/s00436-015-4472-5
  33. Shirakashi S, Morita A, Ishimaru K, Miyashita S. Infection dynamics of Kudoa yasunagai (Myxozoa: Multivalvulida) infecting brain of cultured yellowtail Seriola quinqueradiata in Japan. Dis. Aquat. Org. 2012;101:123-130. https://doi.org/10.3354/dao02513
  34. True K, Purcell MK, Foott JS. Development and validation of a quantitative PCR to detect Parvicapsula minibicornis and comparison to histologically ranked infection of juvenile Chinook salmon, Oncorhynchus tshawytscha (Walbaum), from the Klamath River, USA. J. Fish Dis. 2009;32:183-192. https://doi.org/10.1111/j.1365-2761.2008.00975.x
  35. Wolf K, Markiw ME. Biology contravenes taxonomy in the myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science. 1984;225:1449-1452. https://doi.org/10.1126/science.225.4669.1449
  36. Yanagida T, Sameshima M, Nasu H, Yokoyama H, Ogawa K. Temperature effects on the development of Enteromyxum spp. (Myxozoa) in experimentally infected tiger puffer Takifugu rubripes (Temminck & Schlegel). J. Fish Dis. 2006;29:561-567. https://doi.org/10.1111/j.1365-2761.2006.00752.x
  37. Yokoyama H, Ogawa K, Wakabayashi H. A new collection method of actinosporeans-a probable infective stage of myxosporeans to fishes-from tubificids and experimental infection of goldfish with the actinosporean, Raabeia sp. Fish Pathol. 1991;26:133-138. https://doi.org/10.3147/jsfp.26.133
  38. Yokoyama H, Whipps CM, Kent ML, Mizuno K, Kawakami H. Kudoa thyrsites from Japanese flounder and Kudoa lateolabracis n. sp. from Chinese sea bass: causative myxozoans of post-mortem myoliquefaction. Fish Pathol. 2004;39:79-85. https://doi.org/10.3147/jsfp.39.79
  39. Yokoyama H, Grabner D, Shirakashi S. Transmission biology of the Myxozoa. In: Carvalho ED, David GS, Silva RJ (eds) Health and environment in aquaculture, In Tech, Rijeka, 2012.p. 3−42.
  40. Yokoyama H, Lu M, Mori K, Satoh J, Mekata T, Yoshinaga T. Infection dynamics of Kudoa septempunctata (Myxozoa: Multivalvulida) in hatchery-produced olive flounder Paralichthys olivaceus. Fish Pathol. 2015;50:60-67. https://doi.org/10.3147/jsfp.50.60