Tetracapsuloides: Difference between revisions
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'''''Tetracapsuloides bryosalmonae''''' is a [[myxozoa]]n [[parasite]] of [[salmon]]id fish. It is the only species currently recognized in the monotypic genus '''''Tetracapsuloides'''''. |
'''''Tetracapsuloides bryosalmonae''''' is a [[myxozoa]]n [[parasite]] of [[salmon]]id fish. It is the only species currently recognized in the monotypic genus '''''Tetracapsuloides'''''. The parasite is the cause of Proliferative Kidney Disease (PKD), one of the most serious parasitic diseases of salmonid populations in Europe and North America{{Ref|Hedrick}} that can result in losses of up to 90% in infected populations. ''T. bryosalmonae'' has a two-host life cycle, alternating between freshwater bryozoa and fish. |
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==Taxonomy== |
==Taxonomy== |
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Until the late 1990s, the organism which caused PKD was |
Until the late 1990s, the organism which caused PKD was referred to as '''PKX''' since few details on the organism had been identified. The causative agent of PKD was recognized as a form of Malacosporean{{Ref|Kent1}}, but the absence of mature spores in salmonid hosts, the lack of fish to fish transmission, and seasonality of the disease suggested that the life cycle of PKX was completed in another host and that infection of salmonids could be accidental. |
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Korotneff observed a myxozoan in the [[bryozoa]]n, ''[[Plumatella fungosa]]'', in 1892, which he described as ''Myxosporidium bryozoides''{{Ref|Korotneff}}. 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{{Ref|Anderson}}. The PKX organism was |
Korotneff observed a myxozoan in the [[bryozoa]]n, ''[[Plumatella fungosa]]'', in 1892, which he described as ''Myxosporidium bryozoides''{{Ref|Korotneff}}. 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{{Ref|Anderson}}. The PKX organism was initially described as ''Tetracapsuloides (=Tetracapsuloides) bryosalmonae by'' Canning, Curry, Feist, Longshaw & Okamura 1999{{Ref|Canning1}}, which was assigned to a new [[class (biology)|class]], the [[Malacosporea]] within the [[phylum (biology)|phylum]] [[Myxozoa]]{{Ref|Canning2}}. Around the same time, another group described the PKX organism from [[Arctic char]], ''Salvelinus alpinus'', as ''Tetracapsuloides renicola'' (Kent, Khattra, Hedrick & Devlin 2000){{Ref|Kent2}}, but the first given name has priority according to the rules of the [[binomial nomenclature]]. |
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==Life cycle== |
==Life cycle== |
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''T. bryosalmonae'' has a two-host life cycle, as other myxosporeans, cycling between freshwater bryozoa and salmonid fish species, rather than an [[oligochaete]] or [[polychaete]] [[worm]] |
''T. bryosalmonae'' has a two-host life cycle, as other myxosporeans, cycling between freshwater bryozoa and salmonid fish species, rather than an [[oligochaete]] or [[polychaete]] [[worm]] |
||
as |
as seen in species such as ''[[Myxobolus cerebralis]]''. To date, ''T. bryosalmonae'' has been found to parasitize at last five freshwater bryozoans ''[[Phylactolaemata]]'' species belonging to the genera ''[[Fredericella]]'' and ''[[Plumatella]]'', all considered to be primitive genera{{Ref|Anderson}}. Infected bryozoans release mature T. bryosalmonae malacospores during overt infections when large spore sacs are freely floating within their coelomic cavity {{Ref|Morris}}. Bryozoan dispersal strategies, including colony fragmentation, statoblast dispersal and the formation of migrating zooids allow their colonization of new habitats and the spreading of infective T. bryosalmonae stages {{Ref|Gorgoglione2}}. |
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==Pathology== |
==Pathology and clinical signs== |
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Clinical signs of proliferative kidney disease (PKD) include abdominal swelling and exophthalmia. Internally, is characterized by a swollen [[kidney]] and [[spleen]] associated with the presence of focal grey patches and bloody [[ascites]]. At a late stage in the infection, pale [[gill]]s are indicative of anaemia. Pathology is most evident in species particularly susceptible or naive 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 but results in a vigorous host response in the kidney, inducing a chronic lymphoid hyperplasia marked by a strong parasite-driven immunosuppressant pathogenesis and a dysregulation of T-helper subsets {{Ref|Wang}}{{Ref|Gorgoglione}}{{Ref|Bailey}}. 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. |
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==Distribution== |
==Distribution== |
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''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 [[genotype]]s 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]]''{{Ref|Henderson}}. |
''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 [[genotype]]s 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]]''{{Ref|Henderson}}. |
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PKD is a serious immunopathology causing a high mortality rate, thus with a relevant economic impact for trout aquaculture in Europe and North America. |
PKD is a serious immunopathology causing a high mortality rate, thus with a relevant economic impact for trout aquaculture in Europe and North America. |
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== Impact == |
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Any susceptible fish that are reared on river water with infected bryozoan populations have the potential to be infected with ''T. bryosalmonae''. Naïve fish of any age are considered susceptible. The risk is therefore related to the range of susceptible bryozoan species present. Nutrient enrichment and [[eutrophication]] have been shown to promote bryozoan abundance. Water bodies with high productivity, high temperatures (14°C and above) and typically at lower altitude with a biodiverse macro-fauna with [[Salmonidae|salmonids]] present are more likely habitats for ''F. sultana'' and ''T. bryosalmonae''. Since infective spores are shed from bryozoan colonies for extended periods during the Spring and Summer in particular, the likelihood of individual fish encountering malacospores is high in endemic areas. However, parasite stages released from the fish host are not infectious to fish (no direct fish to fish transmission). Therefore, live fish movements will not lead to direct transmission of the parasite to fish at a new site. However, infected fish may release parasite stages of ''T. bryosalmonae'' that can infect the bryozoan host, if present in the area where the fish are relocated (e.g. a fish farm site). |
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== Diagnosis == |
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Diagnosis is based on clinical signs, the presence of characteristic cells observed by light microscopy in fresh or stained smear, or histological sections of affected kidney, spleen or other affected tissues and organs. Some commercial antibodies are available also for the detection by [[immunohistochemistry]], [[ELISA]] or [[western blot]]. The use of [[Electron microscope|electron microscopy]] can be used to confirm the presence of typical cell within cell arrangements of the parasite and particularly the presence of conspicuous electron lucent organelles in the primary cell. Confirmatory diagnosis is by [[Polymerase chain reaction|PCR]] and subsequent sequencing of the 18S rDNA (Anderson et al., 1999). |
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== Treatments == |
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There are no treatments available for PKD. There are currently no practical cost-effective methods for avoiding or eliminating the infective spores from water flowing into farms. In the UK, some aquaculture production businesses affected by PKD apply a deliberate policy of exposing naïve fish to infected water during the summer (July) so that infection occurs, stimulating an immune response, but clinical disease is avoided because of lower numbers of spores. The following year previously exposed fish show varying degrees of immunity to renewed infection. |
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== Other control strategies == |
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Prevention and control of the disease may be achieved through adoption of a tailored farm management strategy and development of an appropriate production plan. The first requirement is to define whether a farm is at high risk or low risk of infection. Factors to be considered are: Water source (untreated river water high risk vs ground water low risk); Temperature profile of the water over the year; Presence of natural hosts in the water body supplying the farm; Epidemiological situation of other farms in the same catchment area. |
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== Research == |
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Recent advances in analysing the [[transcriptome]] of ''T. bryosalmonae'' in both hosts (bryozoan, fish) have allowed identification of a number of potential virulence factors and vaccine candidates. These molecules are currently being trialed for their effectiveness to provide protection against PKD in farmed trout, following vaccination, in the EU funded Horizon2020 Project [http://www.parafishcontrol.eu/ ParaFishControl]. Increased knowledge of the dysregulated immune response seen in fish during PKD has also highlighted potential ways to reduce the pathology seen, by manipulating aspects of the immune system that control lymphocyte responses. |
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==Cited literature== |
==Cited literature== |
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Revision as of 17:10, 24 February 2020
| Tetracapsuloides | |
|---|---|
Scientific classification 
| |
| Domain: | Eukaryota |
| Kingdom: | Animalia |
| Phylum: | Cnidaria |
| Class: | Malacosporea |
| Order: | Malacovalvulida |
| Family: | Saccosporidae |
| Genus: | Tetracapsuloides Canning, Tops, Curry, Wood & Okamura, 2002 |
| Species: | T. bryosalmonae
|
| Binomial name | |
| Tetracapsuloides bryosalmonae Canning et al., 1999
| |
| Synonyms | |
| |
Tetracapsuloides bryosalmonae is a myxozoan parasite of salmonid fish. It is the only species currently recognized in the monotypic genus Tetracapsuloides. The parasite is the cause of Proliferative Kidney Disease (PKD), one of the most serious parasitic diseases of salmonid populations in Europe and North America[1] that can result in losses of up to 90% in infected populations. T. bryosalmonae has a two-host life cycle, alternating between freshwater bryozoa and fish.
Taxonomy
Until the late 1990s, the organism which caused PKD was referred to as PKX since few details on the organism had been identified. The causative agent of PKD was recognized as a form of Malacosporean[2], but the absence of mature spores in salmonid hosts, the lack of fish to fish transmission, and seasonality of the disease suggested 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[3]. 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[4]. The PKX organism was initially described as Tetracapsuloides (=Tetracapsuloides) bryosalmonae by Canning, Curry, Feist, Longshaw & Okamura 1999[5], which was assigned to a new class, the Malacosporea within the phylum Myxozoa[6]. Around the same time, another group described the PKX organism from Arctic char, Salvelinus alpinus, as Tetracapsuloides renicola (Kent, Khattra, Hedrick & Devlin 2000)[7], 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, as other myxosporeans, cycling between freshwater bryozoa and salmonid fish species, rather than an oligochaete or polychaete worm as seen in species such as Myxobolus cerebralis. To date, T. bryosalmonae has been found to parasitize at last five freshwater bryozoans Phylactolaemata species belonging to the genera Fredericella and Plumatella, all considered to be primitive genera[8]. Infected bryozoans release mature T. bryosalmonae malacospores during overt infections when large spore sacs are freely floating within their coelomic cavity [9]. Bryozoan dispersal strategies, including colony fragmentation, statoblast dispersal and the formation of migrating zooids allow their colonization of new habitats and the spreading of infective T. bryosalmonae stages [10].
Pathology and clinical signs
Clinical signs of proliferative kidney disease (PKD) include abdominal swelling and exophthalmia. Internally, is characterized by a swollen kidney and spleen associated with the presence of focal grey patches and bloody ascites. At a late stage in the infection, pale gills are indicative of anaemia. Pathology is most evident in species particularly susceptible or naive 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 but results in a vigorous host response in the kidney, inducing a chronic lymphoid hyperplasia marked by a strong parasite-driven immunosuppressant pathogenesis and a dysregulation of T-helper subsets [11][12][13]. 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[14]. PKD is a serious immunopathology causing a high mortality rate, thus with a relevant economic impact for trout aquaculture in Europe and North America.
Impact
Any susceptible fish that are reared on river water with infected bryozoan populations have the potential to be infected with T. bryosalmonae. Naïve fish of any age are considered susceptible. The risk is therefore related to the range of susceptible bryozoan species present. Nutrient enrichment and eutrophication have been shown to promote bryozoan abundance. Water bodies with high productivity, high temperatures (14°C and above) and typically at lower altitude with a biodiverse macro-fauna with salmonids present are more likely habitats for F. sultana and T. bryosalmonae. Since infective spores are shed from bryozoan colonies for extended periods during the Spring and Summer in particular, the likelihood of individual fish encountering malacospores is high in endemic areas. However, parasite stages released from the fish host are not infectious to fish (no direct fish to fish transmission). Therefore, live fish movements will not lead to direct transmission of the parasite to fish at a new site. However, infected fish may release parasite stages of T. bryosalmonae that can infect the bryozoan host, if present in the area where the fish are relocated (e.g. a fish farm site).
Diagnosis
Diagnosis is based on clinical signs, the presence of characteristic cells observed by light microscopy in fresh or stained smear, or histological sections of affected kidney, spleen or other affected tissues and organs. Some commercial antibodies are available also for the detection by immunohistochemistry, ELISA or western blot. The use of electron microscopy can be used to confirm the presence of typical cell within cell arrangements of the parasite and particularly the presence of conspicuous electron lucent organelles in the primary cell. Confirmatory diagnosis is by PCR and subsequent sequencing of the 18S rDNA (Anderson et al., 1999).
Treatments
There are no treatments available for PKD. There are currently no practical cost-effective methods for avoiding or eliminating the infective spores from water flowing into farms. In the UK, some aquaculture production businesses affected by PKD apply a deliberate policy of exposing naïve fish to infected water during the summer (July) so that infection occurs, stimulating an immune response, but clinical disease is avoided because of lower numbers of spores. The following year previously exposed fish show varying degrees of immunity to renewed infection.
Other control strategies
Prevention and control of the disease may be achieved through adoption of a tailored farm management strategy and development of an appropriate production plan. The first requirement is to define whether a farm is at high risk or low risk of infection. Factors to be considered are: Water source (untreated river water high risk vs ground water low risk); Temperature profile of the water over the year; Presence of natural hosts in the water body supplying the farm; Epidemiological situation of other farms in the same catchment area.
Research
Recent advances in analysing the transcriptome of T. bryosalmonae in both hosts (bryozoan, fish) have allowed identification of a number of potential virulence factors and vaccine candidates. These molecules are currently being trialed for their effectiveness to provide protection against PKD in farmed trout, following vaccination, in the EU funded Horizon2020 Project ParaFishControl. Increased knowledge of the dysregulated immune response seen in fish during PKD has also highlighted potential ways to reduce the pathology seen, by manipulating aspects of the immune system that control lymphocyte responses.
Cited literature
- ^ 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.
- ^ 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): 254–60. doi:10.1111/j.1550-7408.1985.tb03047.x. PMID 4009511.
{{cite journal}}: Unknown parameter|lastauthoramp=ignored (|name-list-style=suggested) (help) - ^ Korotneff, A. (1892). "Myxosporidium bryozoides". Z. Wiss. Zool. 53: 591–596.
- ^ 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.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ 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.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ 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. doi:10.1111/j.1550-7408.2000.tb00075.x. PMID 11001143.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ 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. doi:10.1645/0022-3395(2000)086[0103:TRNSMS]2.0.CO;2. PMID 10701572.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ 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.
{{cite journal}}: CS1 maint: multiple names: authors list (link) - ^ Morris D.J.; Adams A. (2007). "Sacculogenesis and sporogony of Tetracapsuloides bryosalmonae (Myxozoa: Malacosporea) within the bryozoan host Fredericella sultana (Bryozoa: Phylactolaemata)". Parasitol. Res. 100 (5): 983–992. doi:10.1007/s00436-006-0371-0. PMID 17205353.
- ^ Gorgoglione B.; Kotob M.H.; El-Matbouli M. (2016). "Migrating zooids allow the dispersal of Fredericella sultana (Bryozoa) to escape from unfavourable conditions and further spreading of Tetracapsuloides bryosalmonae". Journal of Invertebrate Pathology. 140: 97–102. doi:10.1016/j.jip.2016.08.010. PMID 27546864.
- ^ 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 (5): 705–715. doi:10.1016/j.fsi.2010.06.016. PMID 20633655.
- ^ 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. PMC 3733943. PMID 23865616.
{{cite journal}}: CS1 maint: unflagged free DOI (link) - ^ Bailey C.; Segner H.; Casanova-Nakayama A; Wahli T. (2017). "Who needs the hotspot? The effect of temperature on the fish host immune response to Tetracapsuloides bryosalmonae the causative agent of proliferative kidney disease". Fish & Shellfish Immunology. 63: 424–437. doi:10.1016/j.fsi.2017.02.039. PMID 28238860.
- ^ 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. doi:10.1098/rspb.2004.2677. PMC 1691782. PMID 15306294.
{{cite journal}}: Unknown parameter|lastauthoramp=ignored (|name-list-style=suggested) (help)
