Folia Parasitologica, vol. 51 (2004), issue 2/3

Folia Parasitologica 51[2/3] 167-176 (2004) | DOI: 10.14411/fp.2004.020

A microsporidian parasite of the genus Spraguea in the nervous tissues of the Japanese anglerfish Lophius litulon

Mark A. Freeman, Hiroshi Yokoyama, Kazuo Ogawa
Department of Aquatic Bioscience, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi 1-1-1, Bunkyo, Tokyo 113-8657, Japan

In the present study, a high percentage of Japanese anglerfish, Lophius litulon (Jordan, 1902), contained a microsporidian infection of the nervous tissues. Xenomas were removed and prepared for standard wax histology and transmission electron microscopy (TEM). DNA extractions were performed on parasite spores and used in PCR and sequencing reactions. Fresh spores measured 3.4 × 1.8 µm and were uniform in size with no dimorphism observed. TEM confirmed that only a single developmental cycle and a single spore form were present. Small subunit (SSU) rDNA sequences were >99.5% similar to those of Spraguea lophii (Doflein, 1898) and Glugea americanus (Takvorian et Cali, 1986) from the European and American Lophius spp. respectively. The microsporidian from the nervous tissue of L. litulon undoubtedly belongs in the genus Spraguea Sprague et Vávra, 1976 and the authors suggest a revision to the generic description of Spraguea to include monomorphic forms and the transfer of Glugea americanus to Spraguea americana comb. n. Since no major differences in ultrastructure or SSU rDNA sequence data exist between Spraguea americana and the microsporidian from the Japanese anglerfish, they evidently belong to the same species. This report of Spraguea americana is the first report of a Spraguea species from L. litulon and indeed from the Pacific water mass.

Keywords: Spraguea, microsporidia, Lophius, nervous tissue

Received: January 5, 2004; Accepted: May 27, 2004; Published: June 1, 2004


References

  1. ALTSCHUL S.F., GISH W., MILLER W., MYERS E.W., LIPMAN D.J. 1990: Basic local alignment search tool. J. Mol. Biol. 215: 403-410 Go to original source... Go to PubMed...
  2. AMIGO J.M., SALVADO H., GRACIA M.P., VIVARES C.P. 1996: Ultrastructure and development of Microsporidium ovoideum (Thelohan, 1895) Sprague, 1977, a microsporidian parasite of the red band fish (Cepola macrophthalma L.). Eur. J. Protistol. 32: 532-538 Go to original source...
  3. ASAHIDA T., KOBAYASHI T., SAITOH K., NAKAYMA I. 1996: Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentrations of urea. Fish. Sci. 62: 727-730
  4. DOFLEIN F. 1898: Studien zur Naturgeschichte der Protozoen. III. Ueber die Myxosporidien. Zool. Jahrb. Abt. Anat. 11: 281-350
  5. HINKLE G., MORRISON H., SOGIN M. 1997: Genes coding for reverse transcriptase, DNA-directed RNA polymerase, and chitin synthase from the microsporidian Spraguea lophii. Biol. Bull. (Woods Hole) 193: 250-251 Go to original source...
  6. JAKOWSKA S. 1964: Infeccao microsporidea das celulas nervosas numa populacao de peixes marinho, Lophius americanus. An. 2nd Congr. Lat.-Am. Zool. 1: 265-273
  7. JAKOWSKA S. 1966: Infection with neurotropic microsporidians in South American Lophius. Trans. Am. Microsc. Soc. 85: 161-162
  8. LOMJ., NILSEN F. 2003: Fish microsporidia: fine structural diversity and phylogeny. Int. J. Parasitol. 33: 107-127 Go to original source... Go to PubMed...
  9. LOUBES C., MAURAND J., ORMIERES R. 1979: Etude ultrastructurale de Spraguea lophii (Doflein, 1898), microsporidie parasite de la Baudroie: essai d'interpretation du dimorphisme sporal. Protistologica 15: 43-54
  10. MAILLO P.A., AMIGO J.M., BAENA R., SALVADO H., GRACIA M.P. 1998: Tetramicra brevifilum (Matthews & Matthews, 1980) (Microsporida: Tetamicriidae) in a new fish host, Lophius budegassa (Spinola, 1807) in Spain. Parasitol. Res. 84: 208-212 Go to original source...
  11. MATTHEWS R.A., MATTHEWS B.F. 1980: Cell and tissue reactions of turbot Scophthalmus maximus (L.) to Tetramicra brevifilum gen. n., sp. n. (Microspora). J. Fish Dis. 3: 495-515 Go to original source...
  12. MONIEZ R. 1887: Observations pour la revision des Microsporidies. C. R. Acad. Sci. 104: 1312-1314
  13. MRAZEK A. 1899: Sporozoenstudien II. Glugea lophii Doflein. Sitzungsber. Koenigl. Boehm. Ges. Wiss., Math.Naturwiss. Cl., Prag 34: 1-8
  14. NILSEN F. 1999: Small subunit rDNA phylogeny of Bacillidium sp. (Microspora: Mrazekiidae) infecting oligochaetes. Parasitology 118: 553-558 Go to original source... Go to PubMed...
  15. NILSEN F. 2000: Small subunit ribosomal DNA phylogeny of microsporidia with particular reference to genera that infect fish. J. Parasitol. 86: 128-133 Go to original source... Go to PubMed...
  16. PACE D. 1908: Parasiten und Pseudoparasiten der Nervenzelle. Vorlaeufige Mitteilungen ueber vergleichende Parasitologie des Nervensystems. Z. Hyg. 60: 62-74 Go to original source...
  17. PAGE R.D.M. 1996: TREEVIEW: An application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12: 357-358 Go to PubMed...
  18. POMPORT-CASTILLON C., ROMESTAND B., De JONCKHEERE J.F. 1997: Identification and phylogenetic relationship of microsporidia by riboprinting. J. Eukaryot. Microbiol. 44: 540-544 Go to original source... Go to PubMed...
  19. POMPORT-CASTILLON C., De JONCKHEERE J.F., ROMESTAND B. 2000: Ribosomal DNA sequences of Glugea anomala, G. stephani, G. americanus and Spraguea lophii (Microsporidia): phylogenetic reconstruction. Dis. Aquat. Org. 40: 125-129 Go to original source... Go to PubMed...
  20. SAITOU N., NEI M. 1987: The neighbour joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425 Go to PubMed...
  21. SANGER F., NICKLEN S., COULSON A.R. 1977: DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74: 5463-5467 Go to original source...
  22. TAKVORIAN P., CALI A. 1986: The ultrastructure of spores (Protozoa: Microsporidia) from Lophius americanus, the anglerfish. J. Protozool. 33: 570-575 Go to original source... Go to PubMed...
  23. THELOHAN P. 1895: Recherches sur les myxosporidies. Bull. Sci. Fr. Belg. 26: 100-394
  24. THOMPSON J.D., GIBSON T.J., PLEWNIAK F., JEANMOUGIN F., HIGGINS D.G. 1997: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24: 4876-4882 Go to original source... Go to PubMed...
  25. WEISSENBERG R. 1909: Beitraege zur Kenntnis von Glugea lophii Doflein. I. Ueber den Sitz und die Verbreitung der Mikrosporidien-Zysten am Nervensystem von Lophius piscatorius und L. budegassa. Sitzungsber. Ges. Naturforsch. Freunde Berlin 9: 557-567
  26. WEISSENBERG R. 1911a: Ueber einige Mikrosporidien aus Fischen (Nosema lophii Doflein, Glugea anomala Moniez, Glugea hertwigii nov. spec.). Sitzungsber. Ges. Naturforsch. Freunde Berlin. 8: 344-357
  27. WEISSENBERG R. 1911b: Beitraege zur Kenntnis von Glugea lophii Doflein. II. Ueber den Bau der Zysten und die Beziehungen zwischen Parasit und Wirtsgewebe. Sitzungsber. Ges. Naturforsch. Freunde Berlin. 3: 149-157
  28. WEISSENBERG R. 1911c: Ueber Mikrosporidien aus dem Nervensystem von Fischen (Glugea lophii Doflein) und die Hypertrophie der befallenen Ganglienzellen. Arch. Mikrosk. Anat. 78: 383-421 Go to original source...
  29. WEISSENBERG R. 1976: Microsporidian interactions with the host cell. In: L.A. Bulla and T.C. Cheng (Eds.), Comparative Pathobiology. Volume I. Plenum Press, New York and London, pp. 203-237
  30. YOKOYAMA H., KIM J., SATO J., SANO M., HIRANO K. 1996: Fluorochrome Uvitex 2B stain for detection of the microsporidian causing beko disease of yellowtail and goldstriped amberjack juveniles. Fish Pathol. 31: 99-104 Go to original source...