Abstract
Salmonid proliferative kidney disease (PKD) is caused by the myxozoan Tetracapsuloides bryosalmonae. Given the serious and apparently growing impact of PKD on farmed and wild salmonids, we undertook a phylogeographic study to gain insights into the history of genealogical lineages of T. bryosalmonae in Europe and North America, and to determine if the global expansion of rainbow trout farming has spread the disease. Phylogenetic analyses of internal transcribed spacer 1 sequences revealed a clade composed of all North American sequences plus a subset of Italian and French sequences. High genetic diversity in North America and the absence of genotypes diagnostic of the North American clade in the rest of Europe imply that southern Europe was colonized by immigration from North America; however, sequence divergence suggests that this colonization substantially pre-dated fisheries activities. Furthermore, the lack of southern European lineages in the rest of Europe, despite widespread rainbow trout farming, indicates that T. bryosalmonae is not transported through fisheries activities. This result strikingly contrasts with the commonness of fisheries-related introductions of other pathogens and parasites and indicates that fishes may be dead-end hosts. Our results also demonstrate that European strains of T. bryosalmonae infect and induce PKD in rainbow trout introduced to Europe.
Full Text
The Full Text of this article is available as a PDF (120.3 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Anderson C. L., Canning E. U., Okamura B. Molecular data implicate bryozoans as hosts for PKX (phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa. Parasitology. 1999 Dec;119(Pt 6):555–561. doi: 10.1017/s003118209900520x. [DOI] [PubMed] [Google Scholar]
- Attwood S. W., Upatham E. S., Meng X. H., Qiu D. C., Southgate V. R. The phylogeography of Asian Schistosoma (Trematoda: Schistosomatidae). Parasitology. 2002 Aug;125(Pt 2):99–112. doi: 10.1017/s0031182002001981. [DOI] [PubMed] [Google Scholar]
- Canning E. U., Curry A., Feist S. W., Longshaw M., Okamura B. A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism). J Eukaryot Microbiol. 2000 Sep-Oct;47(5):456–468. doi: 10.1111/j.1550-7408.2000.tb00075.x. [DOI] [PubMed] [Google Scholar]
- Daszak P., Cunningham A. A., Hyatt A. D. Emerging infectious diseases of wildlife--threats to biodiversity and human health. Science. 2000 Jan 21;287(5452):443–449. doi: 10.1126/science.287.5452.443. [DOI] [PubMed] [Google Scholar]
- Desprès L., Imbert-Establet D., Monnerot M. Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Mol Biochem Parasitol. 1993 Aug;60(2):221–229. doi: 10.1016/0166-6851(93)90133-i. [DOI] [PubMed] [Google Scholar]
- Feist S. W., Longshaw M., Canning E. U., Okamura B. Induction of proliferative kidney disease (PKD) in rainbow trout Oncorhynchus mykiss via the bryozoan Fredericella sultana infected with Tetracapsula bryosalmonae. Dis Aquat Organ. 2001 May 4;45(1):61–68. doi: 10.3354/dao045061. [DOI] [PubMed] [Google Scholar]
- Freeland J. R., Romualdi C., Okamura B. Gene flow and genetic diversity: a comparison of freshwater bryozoan populations in Europe and North America. Heredity (Edinb) 2000 Nov;85(Pt 5):498–508. doi: 10.1046/j.1365-2540.2000.00780.x. [DOI] [PubMed] [Google Scholar]
- Gay M., Okamura B., de Kinkelin P. Evidence that infectious stages of Tetracapsula bryosalmonae for rainbow trout Oncorhynchus mykiss are present throughout the year. Dis Aquat Organ. 2001 Aug 22;46(1):31–40. doi: 10.3354/dao046031. [DOI] [PubMed] [Google Scholar]
- Gilbert Michael A., Granath Willard O., Jr Whirling disease of salmonid fish: life cycle, biology, and disease. J Parasitol. 2003 Aug;89(4):658–667. doi: 10.1645/GE-82R. [DOI] [PubMed] [Google Scholar]
- Harris D. J., Crandall K. A. Intragenomic variation within ITS1 and ITS2 of freshwater crayfishes (Decapoda: Cambaridae): implications for phylogenetic and microsatellite studies. Mol Biol Evol. 2000 Feb;17(2):284–291. doi: 10.1093/oxfordjournals.molbev.a026308. [DOI] [PubMed] [Google Scholar]
- Harvell C. D., Kim K., Burkholder J. M., Colwell R. R., Epstein P. R., Grimes D. J., Hofmann E. E., Lipp E. K., Osterhaus A. D., Overstreet R. M. Emerging marine diseases--climate links and anthropogenic factors. Science. 1999 Sep 3;285(5433):1505–1510. doi: 10.1126/science.285.5433.1505. [DOI] [PubMed] [Google Scholar]
- Hedrick R. P., Baxa D. V., De Kinkelin P., Okamura B. Malacosporean-like spores in urine of rainbow trout react with antibody and DNA probes to Tetracapsuloides bryosalmonae. Parasitol Res. 2003 Nov 11;92(1):81–88. doi: 10.1007/s00436-003-0986-3. [DOI] [PubMed] [Google Scholar]
- Hedrick R. P., el-Matbouli M., Adkison M. A., MacConnell E. Whirling disease: re-emergence among wild trout. Immunol Rev. 1998 Dec;166:365–376. doi: 10.1111/j.1600-065x.1998.tb01276.x. [DOI] [PubMed] [Google Scholar]
- Hewitt G. The genetic legacy of the Quaternary ice ages. Nature. 2000 Jun 22;405(6789):907–913. doi: 10.1038/35016000. [DOI] [PubMed] [Google Scholar]
- Hillis D. M., Dixon M. T. Ribosomal DNA: molecular evolution and phylogenetic inference. Q Rev Biol. 1991 Dec;66(4):411–453. doi: 10.1086/417338. [DOI] [PubMed] [Google Scholar]
- Kent M. L., Hedrick R. P. PKX, the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa. J Protozool. 1985 May;32(2):254–260. doi: 10.1111/j.1550-7408.1985.tb03047.x. [DOI] [PubMed] [Google Scholar]
- Okamura B., Anderson C. L., Longshaw M., Feist S. W., Canning E. U. Patterns of occurrence and 18S rDNA sequence variation of PKX (Tetracapsula bryosalmonae), the causative agent of salmonid proliferative kidney disease. J Parasitol. 2001 Apr;87(2):379–385. doi: 10.1645/0022-3395(2001)087[0379:POOARS]2.0.CO;2. [DOI] [PubMed] [Google Scholar]
- Rappole J. H., Hubálek Z. Migratory birds and West Nile virus. J Appl Microbiol. 2003;94 (Suppl):47S–58S. doi: 10.1046/j.1365-2672.94.s1.6.x. [DOI] [PubMed] [Google Scholar]
- Saulnier D., Philippe H., de Kinkelin P. Molecular evidence that the proliferative kidney disease organism unknown (PKX) is a myxosporean. Dis Aquat Organ. 1999 May 31;36(3):209–212. doi: 10.3354/dao036209. [DOI] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tops Sylvie, Okamura Beth. Infection of bryozoans by Tetracapsuloides bryosalmonae at sites endemic for salmonid proliferative kidney disease. Dis Aquat Organ. 2003 Dec 29;57(3):221–226. doi: 10.3354/dao057221. [DOI] [PubMed] [Google Scholar]
- Vogler A. P., DeSalle R. Evolution and phylogenetic information content of the ITS-1 region in the tiger beetle Cicindela dorsalis. Mol Biol Evol. 1994 May;11(3):393–405. doi: 10.1093/oxfordjournals.molbev.a040121. [DOI] [PubMed] [Google Scholar]