Parasitology Research

, Volume 102, Issue 2, pp 219–228 | Cite as

Arrested development of the myxozoan parasite, Myxobolus cerebralis, in certain populations of mitochondrial 16S lineage III Tubifex tubifex

  • D. V. Baxa
  • G. O. Kelley
  • K. S. Mukkatira
  • K. A. Beauchamp
  • C. Rasmussen
  • R. P. Hedrick
Original Paper

Abstract

Laboratory populations of Tubifex tubifex from mitochondrial (mt)16S ribosomal DNA (rDNA) lineage III were generated from single cocoons of adult worms releasing the triactinomyxon stages (TAMs) of the myxozoan parasite, Myxobolus cerebralis. Subsequent worm populations from these cocoons, referred to as clonal lines, were tested for susceptibility to infection with the myxospore stages of M. cerebralis. Development and release of TAMs occurred in five clonal lines, while four clonal lines showed immature parasitic forms that were not expelled from the worm (non-TAM producers). Oligochaetes from TAM- and non-TAM-producing clonal lines were confirmed as lineage III based on mt16S rDNA and internal transcribed spacer region 1 (ITS1) sequences, but these genes did not differentiate these phenotypes. In contrast, random amplified polymorphic DNA analyses of genomic DNA demonstrated unique banding patterns that distinguished the phenotypes. Cohabitation of parasite-exposed TAM- and non-TAM-producing phenotypes showed an overall decrease in expected TAM production compared to the same exposure dose of the TAM-producing phenotype without cohabitation. These studies suggest that differences in susceptibility to parasite infection can occur in genetically similar T. tubifex populations, and their coexistence may affect overall M. cerebralis production, a factor that may influence the severity of whirling disease in wild trout populations.

References

  1. Andree KB, El-Matbouli M, Hoffman RW, Hedrick RP (1998) A nested polymerase chain reaction for the detection of genomic DNA of Myxobolus cerebralis in rainbow trout (Oncorhynchus mykiss). Dis Aquat Org 34:145–154PubMedCrossRefGoogle Scholar
  2. Antonio DB, Andree KB, McDowell TS, Hedrick RP (1998) Detection of Myxobolus cerebralis in rainbow trout and oligochaete tissues by using a nonradioactive in situ hybridization (ISH) protocol. J Aquat Anim Health 10:338–347CrossRefGoogle Scholar
  3. Arsan L, Hallett S, Bartholomew J (2007) Tubifex tubifex from Alaska and their susceptibility to Myxobolus cerebralis. J Parasitol 93 (in press)Google Scholar
  4. Baldo L, Ferraguti M (2005) Mixed reproductive strategy in Tubifex tubifex (oligochaeta, tubificidae)? J Exp Zool 303A:168–177CrossRefGoogle Scholar
  5. Beauchamp KA, Kathman RD, McDowell TS, Hedrick RP (2001) Molecular phylogeny of tubificid oligochaetes with special emphasis on Tubifex tubifex (Tubificidae). Mol Phylogenet Evol 19:216–224PubMedCrossRefGoogle Scholar
  6. Beauchamp KA, Gay M, Kelley GO, El-Matbouli M, Kathman RD, Nehring RB, Hedrick RP (2002) Prevalence and susceptibility of infection to Myxobolus cerebralis and genetic differences among populations of Tubifex tubifex. Dis Aquat Org 51:113–121PubMedCrossRefGoogle Scholar
  7. Beauchamp KA, Kelley GO, Nehring RB, Hedrick RP (2005) The severity of whirling disease among wild trout corresponds to the differences in genetic composition of Tubifex tubifex populations in Central Colorado. J Parasitol 91:53–60PubMedCrossRefGoogle Scholar
  8. Beauchamp KA, El-Matbouli M, Gay M, Georgiadis MP, Nehring RB, Hedrick RP (2006) The effect of cohabitation of Tubifex tubifex (Oligochaeta: Tubificidae) populations on infections to Myxobolus cerebralis (Myxozoa: Myxobolidae). J Invertebr Pathol 91:1–8PubMedCrossRefGoogle Scholar
  9. Costello MJ (1996) Development of future cleaner-fish technology and other biological control techniques in fish farming. In: Wilson C, Sayer MDJ, Treasurer JW, Costello MJ (eds) Wrasse: biology and use in aquaculture. Fishing News Books, Oxford, UK, pp 171–184Google Scholar
  10. El-Matbouli M, Hoffmann RW (1998) Light and electron microscopic study on the chronological development of Myxobolus cerebralis in Tubifex tubifex to the actinosporean stage of triactinomyxon. Int J Parasitol 28:195–217PubMedCrossRefGoogle Scholar
  11. El-Matbouli M, McDowell TS, Antonio DB, Andree KB, Hedrick RP (1999) Effect of water temperature on the development, release, and survival of the triactinomyxon. J Parasitol 29:627–641CrossRefGoogle Scholar
  12. Gilbert MA, Granath WO Jr (2001) Persistent infection of Myxobolus cerebralis, the causative agent of whirling disease in Tubifex tubifex. J Parasitol 87:101–107PubMedGoogle Scholar
  13. Granath WO Jr, Gilbert MA (2002) Review: The role of Tubifex tubifex (Annelida: Oligochaete: Tubificidae) in the transmission of Myxobolus cerebralis (Myxozoa, Myxosporea: Myxobolidae) In: Bartholomew JL, Wilson C (eds) Whirling disease: reviews and current topics. American Fisheries Society Symposium Series 29, American Fisheries Society, Bethesda, MD pp 79–85Google Scholar
  14. Hedrick RP, El-Matbouli M (2002) Recent advances with taxonomy, life cycle, and development of Myxobolus cerebralis in the fish and oligochaete hosts. In: Bartholomew JL, Wilson C (eds) Whirling disease: reviews and current topics. American Fisheries Society Symposium Series 29, American Fisheries Society, Bethesda, MD pp 45–53Google Scholar
  15. Hedrick RP, El-Matbouli M, Adkison MA, MacConnell E (1998) Whirling disease: re-emergence among wild trout. Immunol Rev 162:365–376CrossRefGoogle Scholar
  16. Higgins DG, Sharp PM (1989) Fast and sensitive multiple sequence alignments on a microcomputer. Comput Appl Biosci 5:151–153PubMedGoogle Scholar
  17. Hofer B (1903) Ueber die Drehkrankheit der Regenbogenforelle. Allgemeinen Fischerei-Zietung 8:7–8Google Scholar
  18. Hoffman GL (1990) Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. J Aquat Anim Health 2:30–37CrossRefGoogle Scholar
  19. Kent ML, Andree KB, Batholomew JL, El-Matbouli M, Desser S, Xiao C, Devlin RH, Hedrick RP, Khattra L, Palenzuela O, Siddall M (2001) Recent advances in our knowledge of the Myxozoa. J Eukaryot Microbiol 48:395–413PubMedCrossRefGoogle Scholar
  20. Kerans BL, Rasmussen C, Stevens R, Colwell A, Winton JR (2004) Differential propagation of the metazoan parasite Myxobolus cerebralis by Limnodrillus hoffmeisteri, Ilyodrilus templetoni, and genetically distinct strains of Tubifex tubifex. J Parasitol 90:1366–1373PubMedCrossRefGoogle Scholar
  21. MacConnell E, Vincent ER (2002) The effects of Myxobolus cerebralis on the salmonid host. In: Bartholomew JL, Wilson C (eds) Whirling disease: reviews and current topics. American Fisheries Society Symposium Series 29, American Fisheries Society, Bethesda, MD pp 95–107Google Scholar
  22. Markiw ME, Wolf K (1983) Myxosoma cerebralis (Myxozoa: Myxosporea) etiologic agent of salmonid whirling disease requires tubificid worms (Annelida: Oligochaeta) in its life cycle. J Protozool 30:561–564Google Scholar
  23. Nehring RB, Walker PG (1996) Whirling disease in the wild: the new reality in the intermountain west. Fisheries 21:28–30Google Scholar
  24. Nehring RB, Thompson KG, Catanese M (2005) Decline in TAM production in Windy Gap Reservoir: is it linked to major shift in relative abundance of tubificid lineages? 11th Annual Whirling Disease Symposium: “Recipes for Recovery”, Denver, CO, pp 9–10Google Scholar
  25. Nickum D (1999) Whirling disease in the United States: a summary of progress in research and management. Coldwater Conservation Fund, Trout UnlimitedGoogle Scholar
  26. Rasmussen C, Zikovich J, Winton JR, Kerans B (2007) Variability in triactinomyxon production from Tubifex tubifex populations from the same mitochondrial DNA lineage infected with Myxobolus cerebralis, the causative agent of whirling disease in salmonids. J Parasitol (in press)Google Scholar
  27. Rognlie MC, Knapp SE (1998) Myxobolus cerebralis in Tubifex tubifex from a whirling disease epizootic in Montana. J Parasitol 84:711–713PubMedCrossRefGoogle Scholar
  28. Rose JD, Marrs GS, Lewis C, Schisler G (2000) Whirling disease behavior and its relation to pathology of the brain stem and spinal cord in rainbow trout. J Aquat Anim Health 12:107–118CrossRefGoogle Scholar
  29. Slootweg R, Malek EA, McCullough FS (1994) The biological control of snail intermediate hosts of schistosomiasis by fish. Rev Fish Biol Fish 4:67–90CrossRefGoogle Scholar
  30. Steinbach-Elwell LC, Kerans BL, Rasmussen C, Winton JR (2006) Interactions among two strains of Tubifex tubifex (Oligochaeta: Tubificidae) and Myxobolus cerebralis (Myxozoa). Dis Aquat Org 68:131–139CrossRefGoogle Scholar
  31. Stevens RB, Kerans BL, Lemmon JC, Rasmussen C (2001) The effects of Myxobolus cerebralis myxospore dose on triactinomyxon production and biology of Tubifex tubifex from two geographic regions. J Parasitol 87:315–321PubMedGoogle Scholar
  32. Sturmbauer C, Opadiya GB, Niederstatter H, Riedmann A, Dallinger R (1999) Mitochondrial DNA reveals cryptic oligochaete species differing in cadmium resistance. Mol Biol Evol 16:967–974PubMedGoogle Scholar
  33. 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 25:4876–4882PubMedCrossRefGoogle Scholar
  34. Welsch J, McClelland M (1990) Fingerprinting genomes using PCR with arbitrary primers. Nucleic Acids Res 18:7213–7218CrossRefGoogle Scholar
  35. Wolf K, Markiw ME (1984) Biology contravenes taxonomy in the Myxozoa: new discoveries show alternation of invertebrate and vertebrate hosts. Science 225:1449–1452PubMedCrossRefGoogle Scholar
  36. Wolf K, Markiw ME, Hiltunen JK (1986) Salmonid whirling disease: Tubifex tubifex (Muller) identified as the essential oligochaete in the protozoan life cycle. J Fish Dis 9:83–85CrossRefGoogle Scholar
  37. Vincent ER (1996) Whirling disease and wild trout: the Montana experience. Fisheries 21:32–34Google Scholar

Copyright information

© Springer-Verlag 2007

Authors and Affiliations

  • D. V. Baxa
    • 1
  • G. O. Kelley
    • 2
  • K. S. Mukkatira
    • 2
  • K. A. Beauchamp
    • 3
  • C. Rasmussen
    • 4
  • R. P. Hedrick
    • 1
  1. 1.School of Veterinary Medicine, Department of Medicine and EpidemiologyUniversity of CaliforniaDavisUSA
  2. 2.California Department of Fish and GameFish Health LaboratoryRancho CordovaUSA
  3. 3.US Geological Survey, National Fish Health Research LaboratoryLeetown Science CenterKearneysvilleUSA
  4. 4.Western Fisheries Research CenterUnited States Geological SurveySeattleUSA

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