Marine Biology

, Volume 152, Issue 5, pp 1095–1104

Thraustochytrids as novel parasitic protists of marine free-living flatworms: Thraustochytrium caudivorum sp. nov. parasitizes Macrostomum lignano

  • Lukas Schärer
  • Dagmar Knoflach
  • Dita B. Vizoso
  • Gunde Rieger
  • Ursula Peintner
Research Article

Abstract

The Labyrinthulomycota are a relatively poorly studied group of heterotrophic unicellular eukaryotes. They comprise three lineages, labyrinthulids, thraustochytrids, and aplanochytrids, which are all primarily marine organisms and considered to be important components of marine microbial communities. Recently a number of Labyrinthulomycota have been implicated as parasites of marine (but also terrestrial) plants and marine molluscs. Here we describe a new species of thraustochytrid, Thraustochytrium caudivorum sp. nov. that we have isolated from laboratory cultures of Macrostomum lignano (Rhabditophora, Macrostomorpha), a marine free-living flatworm. In these worms T. caudivorum can cause lesions, which start at the tip of the tail plate and which can lead to the dissolution of the posterior part of the animal. Although the worms can frequently cure these lesions and regenerate the lost parts, the lesions can also result in the complete dissolution of the animal. We describe this thraustochytrid based on pure agar cultures and infestations in the worm cultures. Moreover, we describe its pathological effects on the worms and its morphology using both light and electron microscopy. In addition, we report a phylogenetic analysis using a partial 18S rDNA sequence that allows us to place this new species within the thraustochytrids. Finally, we outline a protocol that allows to permanently remove the parasites from infested worm cultures. We conclude that thraustochytrids represent a novel group of parasites of free-living flatworms.

Supplementary material

References

  1. Andersen RA, Berges JA, Harrison PJ, Watanabe MM (2005) Recipes for freshwater and seawater media. In: Andersen RA (ed) Algal culturing techniques. Elsevier, Amsterdam, pp 429–538Google Scholar
  2. Bever JD, Morton J (1999) Heritable variation and mechanisms of inheritance of spore shape within a population of Scutellospora pellucida, an arbuscular mycorrhizal fungus. Am J Bot 86:1209–1216PubMedCrossRefGoogle Scholar
  3. Bigelow DM, Olsen MW, Gilbertson RL (2005) Labyrinthula terrestris sp nov., a new pathogen of turf grass. Mycologia 97:185–190PubMedGoogle Scholar
  4. Bower SM (1987) Labyrinthuloides haliotidis n.sp. (Protozoa, Labyrinthomorpha), a pathogenic parasite of small juvenile abalone in a British Columbia mariculture facility. Can J Zool 65:1996–2007Google Scholar
  5. Bresslau E (1928–1933) Turbellaria. Walter de Gruyter, BerlinGoogle Scholar
  6. Craven KD, Peterson PD, Windham DE, Mitchell TK, Martin SB (2005) Molecular identification of the turf grass rapid blight pathogen. Mycologia 97:160–166PubMedCrossRefGoogle Scholar
  7. Egger B, Ladurner P, Nimeth K, Gschwentner R, Rieger R (2006) The regeneration capacity of the flatworm Macrostomum lignano—on repeated regeneration, rejuvenation, and the minimal size needed for regeneration. Dev Genes Evol 216:565–577PubMedCrossRefGoogle Scholar
  8. Gardes M, Bruns TD (1993) ITS primers with enhanced specificity for basidiomycetes—application to the identification of mycorrhizae and rusts. Mol Ecol 2:113–118PubMedGoogle Scholar
  9. Hallez P (1879) Contributions à l’histoire naturelle des Turbellariés. Trav Inst Zool Lille Wimereux 2:viii+213, 211 platesGoogle Scholar
  10. Jensen PR, Jenkins KM, Porter D, Fenical W (1998) Evidence that a new antibiotic flavone glycoside chemically defends the sea grass Thalassia testudinum against zoosporic fungi. Appl Environ Microb 64:1490–1496Google Scholar
  11. Kuhn G, Hijri M, Sanders IR (2001) Evidence for the evolution of multiple genomes in arbuscular mycorrhizal fungi. Nature 414:745–748PubMedCrossRefGoogle Scholar
  12. Ladurner P, Rieger RM, Baguña J (2000) Spatial distribution and differentiation potential of stem cells in hatchlings and adults in the marine platyhelminth Macrostomum sp.: a bromodeoxyuridine analysis. Dev Biol 226:231–241PubMedCrossRefGoogle Scholar
  13. Ladurner P, Schärer L, Salvenmoser W, Rieger RM (2005) A new model organism among the lower Bilateria and the use of digital microscopy in taxonomy of meiobenthic Platyhelminthes: Macrostomum lignano, n. sp. (Rhabditophora, Macrostomorpha). J Zool Syst Evol Res 43:114–126CrossRefGoogle Scholar
  14. Leander CA, Porter D (2000) Redefining the genus Aplanochytrium (Phylum Labyrinthulomycota). Mycotaxon 76:439–444Google Scholar
  15. Leander CA, Porter D (2001) The Labyrinthulomycota is comprised of three distinct lineages. Mycologia 93:459–464CrossRefGoogle Scholar
  16. Leander CA, Porter D, Leander BS (2004) Comparative morphology and molecular phylogeny of aplanochytrids (Labyrinthulomycota). Eur J Protistol 40:317–328CrossRefGoogle Scholar
  17. Meixner J (1938) Turbellaria (Strudelwürmer) I. Allgemeiner Teil. In: Grimpe G, Wagler E, Remane A (eds) Die Tierwelt der Nord- und Ostsee. Akademischer Verlag, Leipzig, pp 146Google Scholar
  18. Mo CQ, Douek J, Rinkevich B (2002) Development of a PCR strategy for thraustochytrid identification based on 18S rDNA sequence. Mar Biol 140:883–889CrossRefGoogle Scholar
  19. Pawlowska TE, Taylor JW (2004) Organization of genetic variation in individuals of arbuscular mycorrhizal fungi. Nature 427:733–737PubMedCrossRefGoogle Scholar
  20. Ragan MA, MacCallum GS, Murphy CA, Cannone JJ, Gutell RR, McGladdery SE (2000) Protistan parasite QPX of hard-shell clam Mercenaria mercenaria is a member of Labyrinthulomycota. Dis Aquat Organ 42:185–190PubMedCrossRefGoogle Scholar
  21. Raghukumar S (2002) Ecology of the marine protists, the Labyrinthulomycetes (Thraustochytrids and Labyrinthulids). Eur J Protistol 38:127–145CrossRefGoogle Scholar
  22. Rambaut A (1996) Se-Al: Sequence Alignment EditorGoogle Scholar
  23. Rieger RM, Gehlen M, Haszprunar G, Holmlund M, Legniti A, Salvenmoser W, Tyler S (1988) Laboratory cultures of marine Macrostomida (Turbellaria). Fortschr Zool 36:523Google Scholar
  24. Rinkevich B (1999) Cell cultures from marine invertebrates: obstacles, new approaches and recent improvements. J Biotechnol 70:133–153CrossRefGoogle Scholar
  25. Salamin N, Chase MW, Hodkinson TR, Savolainen V (2003) Assessing internal support with large phylogenetic DNA matrices. Mol Phylogenet Evol 51:112–126Google Scholar
  26. Schärer L, Ladurner P (2003) Phenotypically plastic adjustment of sex allocation in a simultaneous hermaphrodite. Proc R Soc Lond B 270:935–941CrossRefGoogle Scholar
  27. Schärer L, Joss G, Sandner P (2004) Mating behaviour of the marine turbellarian Macrostomum sp.: these worms suck. Mar Biol 145:373–380CrossRefGoogle Scholar
  28. Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultrastruct Res 26:31–43PubMedCrossRefGoogle Scholar
  29. Swofford DL (2003) PAUP* phylogenetic analysis using parsimony (*and other methods). Sinauer Associates, SunderlandGoogle Scholar
  30. Tyler S (1981) Development of cilia in embryos of the turbellarian Macrostomum. Hydrobiologia 84:231–239CrossRefGoogle Scholar
  31. Vilgalys R, Hester M (1990) Rapid genetic identification and mapping of enzymatically amplified ribosomal DNA from several Cryptococcus species. J Bacteriol 172:4238–4246PubMedGoogle Scholar
  32. von Graff L (1882) Monographie der Turbellarien. I. Rhabdocoelida. Willhelm Engelmann, LeipzigGoogle Scholar
  33. von Graff L (1903) Die Turbellarien als Parasiten und Wirte. Leuschner & Lubensy’s Universitats-Buchhandlung, GrazGoogle Scholar
  34. White TJ, Bruns TD, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR protocols: a guide to methods and applications. Academic, San Diego, pp 315–322Google Scholar
  35. Zolan ME, Pukkila PJ (1986) Inheritance of DNA methylation in Coprinus cinereus. Mol Cell Biol 6:195–200PubMedGoogle Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • Lukas Schärer
    • 1
    • 3
  • Dagmar Knoflach
    • 1
  • Dita B. Vizoso
    • 1
  • Gunde Rieger
    • 1
  • Ursula Peintner
    • 2
  1. 1.Division of Ultrastructural Research and Evolutionary Biology, Institute of ZoologyUniversity of InnsbruckInnsbruckAustria
  2. 2.Institute of MicrobiologyUniversity of InnsbruckInnsbruckAustria
  3. 3.Evolutionary Biology, Zoological InstituteUniversity of BaselBaselSwitzerland

Personalised recommendations