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Geographical and host distribution patterns of Parvicapsula minibicornis (Myxozoa) small subunit ribosomal RNA genetic types

  • STEPHEN D. ATKINSON (a1) (a2), SIMON R. M. JONES (a3), ROBERT D. ADLARD (a4) and JERRI L. BARTHOLOMEW (a2)

Summary

Parvicapsula minibicornis is a myxozoan parasite implicated in mortalities of both juvenile and pre-spawning adult salmon in the Pacific Northwest of North America. Disease severity and presentation varies between salmon species and geographical localities. To better characterize population structure of the parasite, we sought genetic markers in the P. minibicornis ribosomal RNA gene. We compared samples from California with the type specimen from British Columbia, identified sequence variations, and then sequenced 197 samples from fish, river water and the parasite's polychaete worm host. Although DNA sequences of the parasite were >98·9% similar, there was enough variation to define 15 genotypes. All genotypes were detected in fish samples, although not in all species. A single genotype only was found in sockeye and pink salmon in the Fraser River Basin, but was not detected in sockeye from the adjacent Columbia River Basin. All coho salmon, irrespective of river basin, were infected with a unique mix of 2 genotypes. These data indicated that the P. minibicornis population exhibited strong signals of structuring by both geography and salmonid host species. Particular genotypes may correlate with disease differences seen in salmon populations in the Pacific Northwest.

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Corresponding author

*Corresponding author: Department of Microbiology, Oregon State University, Nash Hall 220, Corvallis, Oregon 97331, USA. Tel: +1 541 737 1856. Fax: +1 541 737 0496. E-mail: bartholj@science.oregonstate.edu

References

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Arsan, E. L., Atkinson, S. D., Hallett, S. L., Meyers, T. and Bartholomew, J. L. (2007). Expanded geographical distribution of Myxobolus cerebralis: first detections from Alaska. Journal of Fish Diseases 30, 483491.
Atkinson, S. D. and Bartholomew, J. L. (2010 a). Disparate infection patterns of Ceratomyxa shasta (Myxozoa) in rainbow trout Oncorhynchus mykiss and Chinook salmon Oncorhynchus tshawytscha correlate with ITS-1 sequence variation in the parasite. International Journal for Parasitology 40, 599604. doi:10.1016/j.ijpara.2009.10.010.
Atkinson, S. D. and Bartholomew, J. L. (2010 b). Spatial, temporal and host factors structure the Ceratomyxa shasta (Myxozoa) population in the Klamath River Basin. Infection, Genetics and Evolution 10, 10191026.
Bartholomew, J. L., Atkinson, S. D. and Hallett, S. L. (2006). Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. Journal of Parasitology 92, 742748.
Bartholomew, J. L., Whipple, M. J., Stevens, D. G. and Fryer, J. L. (1997). The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology 83, 859868.
Bradford, M. J., Lovy, J., Patterson, D., Speare, D. J., Bennett, W. R., Stobbart, A. R. and Tovey, C. P. (2010). Parvicapsula minibicornis infections in gill and kidney and the premature mortality of adult sockeye salmon (Oncorhynchus nerka) from Cultus Lake, British Columbia. Canadian Journal of Fisheries and Aquatic Sciences 67(4), 673683.
Dover, G. A. (1982). Molecular drive: a cohesive mode of species evolution. Nature, London 299, 111117.
Ferguson, J. A., Atkinson, S. D., Whipps, C. M. and Kent, M. L. (2008). Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. Journal of Parasitology 94, 1322–34.
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 15211534.
Foott, J. S., Harmon, R. and Stone, R. (2004). Effect of water temperature on nonspecific immune function and ceratomyxosis in juvenile Chinook salmon and steelhead from the Klamath River. California Fish and Game 90, 7184.
Foott, J. S., Stone, R., Wiseman, E., True, K. and Nichols, K. (2007). Longevity of Ceratomyxa shasta and Parvicapsula minibicornis actinospore infectivity in the Klamath River. Journal of Aquatic Animal Health 19, 7783.
Groot, C. and Margolis, L. (1991). Pacific Salmon Life Histories. 2003 Edn. UBC Press, Vancouver, Canada.
Gunter, N. L., Whipps, C. M. and Adlard, R. D. (2009). Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience? International Journal for Parasitology 39, 13951405. doi:10.1016/j.ijpara. 2009.04.008.
Hall, T. A. (1999). BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.
Hallett, S. L. and Bartholomew, J. L. (2006). Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Diseases of Aquatic Organisms 71, 109118.
Hallett, S. L. and Bartholomew, J. L. (2009). Development and application of a duplex QPCR for river water samples to monitor the myxozoan parasite Parvicapsula minibicornis. Diseases of Aquatic Organisms 86, 3950.
Hazel, C. R. (1966). A note on the freshwater polychaete, Manayunkia speciosa Leidy, from California and Oregon. The Ohio Journal of Science 66, 533535.
Huelsenbeck, J. P. and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754755. doi:10.1093/bioinformatics/17.8.754.
Jones, S. R. M., Prosperi-Porta, G., Dawe, S. C. and Barnes, D. P. (2003). Distribution, prevalence, and severity of Parvicapsula minibicornis infections among anadromous salmonids in the Fraser River, British Columbia, Canada. Diseases of Aquatic Organisms 54, 4952.
Jones, S., Prosperi-Porta, G., Dawe, S., Taylor, K. and Goh, B. (2004). Parvicapsula minibicornis in anadromous sockeye (Oncorhynchus nerka) and coho (Oncorhynchus kisutch) salmon from tributaries of the Columbia River. Journal of Parasitology 90, 882885.
Kent, M. L., Hervio, D. M. L., Docker, M. F. and Devlin, R. H. (1996). Taxonomic studies and diagnostic tests for myxosporean and microsporidian pathogens of salmonid fishes utilising ribosomal DNA sequence. Journal of Eukaryotic Microbiology 43, 98S99S.
Kent, M. L., Khattra, J., Hedrick, R. P. and Devlin, R. H. (2000). Tetracapsula renicola n. sp. (MYXOZOA:SACCOSPORIDAE); The PKX myxozoan – the cause of proliferative kidney disease in salmonid fishes. Journal of Parasitology 86, 103111.
Kent, M. L., Whitaker, D. J. and Dawe, S. C. (1997). Parvicapsula minibicornis n. sp. (Myxozoa, Myxosporea) from the kidney of sockeye salmon (Oncorhynchus nerka) from British Columbia, Canada. Journal of Parasitology 83, 11531156.
Køie, M., Karlsbakk, E. and Nylund, A. (2007). 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. Journal of Parasitology 93, 14591467.
McPhail, J. D. and Lindsey, C. C. (1986). Zoogeography of the freshwater fishes of Cascadia (the Columbia system and rivers north to the Stikine). In Zoogeography of North American Freshwater Fishes (ed. Hocutt, C. H. and Wiley, E. O.), pp. 615637. Wiley and Sons, New York, USA.
Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Sweden.
Raverty, S., Kieser, D., Bagshaw, J. and St-Hilaire, S. (2000). Renal infestation with Parvicapsula minibicornis in wild sockeye salmon from the Harrison and Adams rivers in British Columbia. Canadian Veterinary Journal 41, 317318.
Schlegel, M., Lom, J., Stechmann, A., Bernhard, D., Leipe, D., Dykova, I. and Sogin, M. L. (1996). Phylogenetic analysis of complete small subunit ribosomal RNA coding region of Myxidium lieberkuehni: evidence that Myxozoa are Metazoa and related to the Bilateria. Archiv für Protistenkunde 147, 19.
St-Hilaire, S., Boichuk, M., Barnes, D., Higgins, M., Devlin, R., Withler, R., Khattra, J., Jones, S. and Kieser, D. (2002). Epizootiology of Parvicapsula minibicornis in Fraser River sockeye salmon, Oncorhynchus nerka (Walbaum). Journal of Fish Diseases 25, 107120.
Stocking, R. W., Holt, R. A., Foott, J. S. and Bartholomew, J. L. (2006). Spatial and temporal occurrence of the salmonid parasite Ceratomyxa shasta (Myxozoa) in the Oregon-California Klamath River basin. Journal of Aquatic Animal Health 18, 194202.
Stocking, R. W and Bartholomew, J. L. (2007). Distribution and habitat characteristics of Manayunkia speciosa and infection prevalence with the parasite Ceratomyxa shasta in the Klamath River, Oregon-California. Journal of Parasitology 93, 7888.
Stone, R., Foott, J. S. and Fogerty, R. (2008). FY2006 investigational report: comparative susceptibility to infection and disease from Ceratomyxa shasta and Parvicapsula minibicornis in Klamath River basin juvenile Chinook, coho, and steelhead populations. US Fish and Wildlife Service California-Nevada Fish Health Center, Anderson, CA, USA.
Tamura, K., Dudley, J., Nei, M. and Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24, 15961599. doi: 10.1093/molbev/msm092.
Taylor, E. B., Foote, C. J. and Wood, C. C. (1996). Molecular and genetic evidence for parallel life-history evolution within a Pacific salmon (sockeye salmon and kokanee, Oncorhynchus nerka). Evolution 50, 401416.
True, K., Purcell, M. and Foott, J. S. (2009). 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. Journal of Fish Diseases 32, 183192.

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