Tetracapsuloides bryosalmonae

Tetracapsuloides bryosalmonae is a myxozoan parasite of salmonid fish. It causes Proliferative Kidney Disease (PKD), one of the most serious parasitic diseases of salmonid populations in Europe and North America, which causes losses of up to 90% in infected populations.

Taxonomy

Until the late 1990s, the organism which caused PKD was enigmatic. The "PKX organism", the causative agent of the disease, had been recognized as some form of Malacosporean, but the absence of mature spores in salmonid hosts, the lack of fish to fish transmission, and seasonality of the disease suggest that the life cycle of PKX was completed in another host and that infection of salmonids could be accidental. Korotneff observed a myxozoan in the bryozoan, Plumatella fungosa, in 1892, which he described as Myxosporidium bryozoides. Myxozoan infection of bryozoans was not reported again until 1996. Ecological investigations of freshwater bryozoans in North America discovered parasitic sacs of a myxozoan species, freely floating in the body cavities of several bryozoans. Molecular analyses indicated that the 18S rDNA sequences of these sacs were indistinguishable from those of PKX, and the PKX organism was scientifically described as Tetracapsuloides bryosalmonae Canning, Curry, Feist, Longshaw & Okamura 1999, which has been assigned to a new class, the Malacosporea within the phylum Myxozoa. Around the same time, another group described the PKX organism from Arctic char, Salvelinus alpinus, as Tetracapsuloides renicola Kent, Khattra, Hedrick & Devlin 2000, but the first given name has priority according to the rules of the binomial nomenclature.

Life cycle

T. bryosalmonae has a two-host life cycle, although it is highly unusual among the myxosporea, cycling between freshwater bryozoa and salmonid fish species, rather than an oligochaete or polychaete worm. To date, T. bryosalmonae has been found to parasitize five bryozoan species belonging to the genera Fredericella and Plumatella, all considered to be primitive genera.

Pathology

Proliferative kidney disease (PKD) is characterised by a swollen kidney and spleen, bloody ascites, and pale gills, which indicate the fish becomes anemic at the late stage of the disease. Note that those symptoms are common amongst many other fish diseases and do not specifically indicate an infection with Tetracapsuloides bryosalmonae. It is important to clarify the pathologic condition only happens in species particularly susceptible or naïve to T. bryosalmonae. In those cases, the parasite is allowed to cross the renal tubules wall to proliferate within the interstitial tissue of kidney (=histozoic proliferation). This proliferation stage is a dead end for the parasite (=extrasporogonic proliferation) but instead causes a tumultuous tumour-like tissue reaction in the kidney, inducing a chronic lymphoid hyperplasia marked by a strong parasite-driven immunosuppressant pathogenesis and with a dysregulation of T-helper lymphocyte subsets . In advanced pathology stages, this chronic lymphoid hyperplasia causes the development of granulomatous-like lesions, thus resulting in the characteristic swelling of the whole kidney.

Distribution

T. bryosalmonae has been recorded in Europe and North America. 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 which are characteristic of the North American clade in the rest of Europe implies that southern Europe was colonized by immigration from North America; however, sequence divergence suggests that this colonization substantially pre-dated human movements of fish. 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 contrasts with the commonness of fisheries-related introductions of other pathogens and parasites such as Myxobolus cerebralis and Ceratomyxa shasta. PKD is a serious immunopathology causing a high mortality rate, thus with a relevant economic impact for trout aquaculture in Europe and North America.

Cited literature

1. ^ Hedrick R.; McConnell E.; de Kinkelin P (1993). "Proliferative kidney disease of salmonid fish". Annual Review of Fish Diseases. 3: 277–290. doi:10.1016/0959-8030(93)90039-E. 
2. ^ Kent, M.L. & R.P. Hedrick (1985). "PKX the causative agent of proliferative kidney disease (PKD) in Pacific salmonid fishes and its affinities with the Myxozoa". Journal of Protozoology. 32 (2): 254 260. PMID 4009511. doi:10.1111/j.1550-7408.1985.tb03047.x. 
3. ^ Korotneff, A. (1892). "Myxosporidium bryozoides". Z. Wiss. Zool. 53: 591–596. 
4. ^ Anderson, C.L., Canning, E.U. & Okamura, B. (1999). "18S rDNA sequences indicate that PKX organism parasitizes Bryozoa". Bulletin of the European Association of Fish Pathologists. 19: 94–97. CS1 maint: Multiple names: authors list (link)
5. ^ Canning, E.U., Curry, A., Feist, S.W., Longshaw, M., & Okamura, B. (1999). "Tetracapsula bryosalmonae n.sp. for PKX organism the cause of PKD in salmonid fish". Bulletin of the European Association of Fish Pathologists. 19 (2): 203–206. CS1 maint: Multiple names: authors list (link)
6. ^ Canning, E.U., Curry, A., Feist, S.W., Longshaw, M., & Okamura, B. (2000). "A new class and order of myxozoans to accommodate parasites of bryozoans with ultrastructural observations on Tetracapsula bryosalmonae (PKX organism)". Journal of Eukaryotic Microbiology. 47 (5): 456–468. PMID 11001143. doi:10.1111/j.1550-7408.2000.tb00075.x. CS1 maint: Multiple names: authors list (link)
7. ^ Kent, M.L. J. Khattra, R.P. Hedrick, and R.H. Devlin (2000). "Tetracapsula renicola (Myxozoa: Saccosporidae); the PKX myxozoan – the cause of proliferative kidney disease of salmonid fishes". Journal of Parasitology. 86 (1): 103–111. PMID 10701572. doi:10.1645/0022-3395(2000)086[0103:TRNSMS]2.0.CO;2. CS1 maint: Multiple names: authors list (link)
8. ^ Anderson, C.L., Canning, E.U. & Okamura, B. (1999). "18S rDNA sequences indicate that PKX organism parasitizes Bryozoa". Bulletin of the European Association of Fish Pathologists. 19: 94–97. CS1 maint: Multiple names: authors list (link)
9. ^ Wang T.; Holland J.W.; Martin S.A.; Secombes C.J. (2010). "Sequence and expression analysis of two T helper master transcription factors, T-bet and GATA3, in rainbow trout Oncorhynchus mykiss and analysis of their expression during bacterial and parasitic infection". Fish and Shellfish Immunology. 29: 705–715. doi:10.1016/j.fsi.2010.06.016. 
10. ^ Gorgoglione B.; Wang T.; Secombes C.J.; Holland J.W. (2013). "Immune gene expression profiling of Proliferative Kidney Disease in rainbow trout Oncorhynchus mykiss reveals a dominance of anti-inflammatory, antibody and T helper cell-like activities". Veterinary Research. 44: 55. doi:10.1186/1297-9716-44-55. 
11. ^ Henderson, M. & Okamura, B. (2004). "The phylogeography of salmonid proliferative kidney disease in Europe and North America". Proceedings of the Royal Society B. 271 (1549): 1729–1736. PMC 1691782 . PMID 15306294. doi:10.1098/rspb.2004.2677.