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Molecular identification and transmission studies of X-cell parasites from Atlantic cod Gadus morhua (Gadiformes: Gadidae) and the northern black flounder Pseudopleuronectes obscurus (Pleuronectiformes: Pleuronectidae).

Freeman MA, Eydal M, Yoshimizu M, Watanabe K, Shinn AP, Miura K, Ogawa K - Parasit Vectors (2011)

Bottom Line: The inability to successfully transmit both parasites in this study suggests that either host detachment combined with a period of independent development or an alternate host is required to complete the life cycle for X-cell parasites.Phylogenetic analyses of SSU rDNA confirm a monophyletic grouping for all sequenced X-cell parasites, but do not robustly support their placement within any established protist phylum.Analysis of SSU rDNA from X-cells in Japanese flatfish reveals that the same parasite can infect more than one species of fish.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Ocean and Earth Sciences & Institute of Biological Sciences, University of Malaya, Kuala Lumpur, Malaysia. mark@um.edu.my

ABSTRACT

Background: Epidermal pseudotumours from Hippoglossoides dubius and Acanthogobius flavimanus in Japan and gill lesions in Limanda limanda from the UK have been shown to be caused by phylogenetically related protozoan parasites, known collectively as X-cells. However, the phylogenetic position of the X-cell group is not well supported within any of the existing protozoan phyla and they are currently thought to be members of the Alveolata.Ultrastructural features of X-cells in fish pseudotumours are somewhat limited and no typical environmental stages, such as spores or flagellated cells, have been observed. The life cycles for these parasites have not been demonstrated and it remains unknown how transmission to a new host occurs. In the present study, pseudobranchial pseudotumours from Atlantic cod, Gadus morhua, in Iceland and epidermal pseudotumours from the northern black flounder, Pseudopleuronectes obscurus, in Japan were used in experimental transmission studies to establish whether direct transmission of the parasite is achievable. In addition, X-cells from Atlantic cod were sequenced to confirm whether they are phylogenetically related to other X-cells and epidermal pseudotumours from the northern black flounder were analysed to establish whether the same parasite is responsible for infecting different flatfish species in Japan.

Results: Phylogenetic analyses of small subunit ribosomal DNA (SSU rDNA) sequence data from Atlantic cod X-cells show that they are a related parasite that occupies a basal position to the clade containing other X-cell parasites. The X-cell parasite causing epidermal pseudotumours in P. obscurus is the same parasite that causes pseudotumours in H. dubius. Direct, fish to fish, transmission of the X-cell parasites used in this study, via oral feeding or injection, was not achieved. Non-amoeboid X-cells are contained within discrete sac-like structures that are loosely attached to epidermal pseudotumours in flatfish; these X-cells are able to tolerate exposure to seawater. A sensitive nested PCR assay was developed for the sub clinical detection of both parasites and to assist in future life cycle studies. PCR revealed that the parasite in P. obscurus was detectable in non-pseudotumourous areas of fish that had pseudotumours present in other areas of the body.

Conclusions: The inability to successfully transmit both parasites in this study suggests that either host detachment combined with a period of independent development or an alternate host is required to complete the life cycle for X-cell parasites. Phylogenetic analyses of SSU rDNA confirm a monophyletic grouping for all sequenced X-cell parasites, but do not robustly support their placement within any established protist phylum. Analysis of SSU rDNA from X-cells in Japanese flatfish reveals that the same parasite can infect more than one species of fish.

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Proposed life cycle for the X-cell parasite from flatfish in northern Japan. The proposed life cycle consists of four stages. (I) An infective stage, either flagellated or equipped with suitable apparatus for host penetration/infection, which is released into the environment to infect a fish host. (II) A proliferative cycle starts in the fish which develops into large epidermal pseudotumours. (III) As the pseudotumours mature, sac-like extremities are lost from the host fish and fall to the seabed where the X-cells are released into the substrate. (IV) In the substrate, either a free-living development occurs or the X-cells find an alternate host where development proceeds.
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Figure 7: Proposed life cycle for the X-cell parasite from flatfish in northern Japan. The proposed life cycle consists of four stages. (I) An infective stage, either flagellated or equipped with suitable apparatus for host penetration/infection, which is released into the environment to infect a fish host. (II) A proliferative cycle starts in the fish which develops into large epidermal pseudotumours. (III) As the pseudotumours mature, sac-like extremities are lost from the host fish and fall to the seabed where the X-cells are released into the substrate. (IV) In the substrate, either a free-living development occurs or the X-cells find an alternate host where development proceeds.

Mentions: We do not believe that fish represent a dead-end or incidental host for X-cells. X-cells have evolved very specific tissue tropisms in the fish species they infect and have been reported from 5 teleost orders globally [1], suggesting a long-term and well-established host parasite relationship. Therefore, we can conclude that X-cell development in the fish host is purely a proliferative phase that leads to further development either outside of the fish host or in an alternate host. The lack of direct transmission for the X-cell parasites in this study supports this theory. Figure 7 shows four proposed stages in the life cycle for the X-cell parasite infecting flatfish in northern Japan.


Molecular identification and transmission studies of X-cell parasites from Atlantic cod Gadus morhua (Gadiformes: Gadidae) and the northern black flounder Pseudopleuronectes obscurus (Pleuronectiformes: Pleuronectidae).

Freeman MA, Eydal M, Yoshimizu M, Watanabe K, Shinn AP, Miura K, Ogawa K - Parasit Vectors (2011)

Proposed life cycle for the X-cell parasite from flatfish in northern Japan. The proposed life cycle consists of four stages. (I) An infective stage, either flagellated or equipped with suitable apparatus for host penetration/infection, which is released into the environment to infect a fish host. (II) A proliferative cycle starts in the fish which develops into large epidermal pseudotumours. (III) As the pseudotumours mature, sac-like extremities are lost from the host fish and fall to the seabed where the X-cells are released into the substrate. (IV) In the substrate, either a free-living development occurs or the X-cells find an alternate host where development proceeds.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3045979&req=5

Figure 7: Proposed life cycle for the X-cell parasite from flatfish in northern Japan. The proposed life cycle consists of four stages. (I) An infective stage, either flagellated or equipped with suitable apparatus for host penetration/infection, which is released into the environment to infect a fish host. (II) A proliferative cycle starts in the fish which develops into large epidermal pseudotumours. (III) As the pseudotumours mature, sac-like extremities are lost from the host fish and fall to the seabed where the X-cells are released into the substrate. (IV) In the substrate, either a free-living development occurs or the X-cells find an alternate host where development proceeds.
Mentions: We do not believe that fish represent a dead-end or incidental host for X-cells. X-cells have evolved very specific tissue tropisms in the fish species they infect and have been reported from 5 teleost orders globally [1], suggesting a long-term and well-established host parasite relationship. Therefore, we can conclude that X-cell development in the fish host is purely a proliferative phase that leads to further development either outside of the fish host or in an alternate host. The lack of direct transmission for the X-cell parasites in this study supports this theory. Figure 7 shows four proposed stages in the life cycle for the X-cell parasite infecting flatfish in northern Japan.

Bottom Line: The inability to successfully transmit both parasites in this study suggests that either host detachment combined with a period of independent development or an alternate host is required to complete the life cycle for X-cell parasites.Phylogenetic analyses of SSU rDNA confirm a monophyletic grouping for all sequenced X-cell parasites, but do not robustly support their placement within any established protist phylum.Analysis of SSU rDNA from X-cells in Japanese flatfish reveals that the same parasite can infect more than one species of fish.

View Article: PubMed Central - HTML - PubMed

Affiliation: Institute of Ocean and Earth Sciences & Institute of Biological Sciences, University of Malaya, Kuala Lumpur, Malaysia. mark@um.edu.my

ABSTRACT

Background: Epidermal pseudotumours from Hippoglossoides dubius and Acanthogobius flavimanus in Japan and gill lesions in Limanda limanda from the UK have been shown to be caused by phylogenetically related protozoan parasites, known collectively as X-cells. However, the phylogenetic position of the X-cell group is not well supported within any of the existing protozoan phyla and they are currently thought to be members of the Alveolata.Ultrastructural features of X-cells in fish pseudotumours are somewhat limited and no typical environmental stages, such as spores or flagellated cells, have been observed. The life cycles for these parasites have not been demonstrated and it remains unknown how transmission to a new host occurs. In the present study, pseudobranchial pseudotumours from Atlantic cod, Gadus morhua, in Iceland and epidermal pseudotumours from the northern black flounder, Pseudopleuronectes obscurus, in Japan were used in experimental transmission studies to establish whether direct transmission of the parasite is achievable. In addition, X-cells from Atlantic cod were sequenced to confirm whether they are phylogenetically related to other X-cells and epidermal pseudotumours from the northern black flounder were analysed to establish whether the same parasite is responsible for infecting different flatfish species in Japan.

Results: Phylogenetic analyses of small subunit ribosomal DNA (SSU rDNA) sequence data from Atlantic cod X-cells show that they are a related parasite that occupies a basal position to the clade containing other X-cell parasites. The X-cell parasite causing epidermal pseudotumours in P. obscurus is the same parasite that causes pseudotumours in H. dubius. Direct, fish to fish, transmission of the X-cell parasites used in this study, via oral feeding or injection, was not achieved. Non-amoeboid X-cells are contained within discrete sac-like structures that are loosely attached to epidermal pseudotumours in flatfish; these X-cells are able to tolerate exposure to seawater. A sensitive nested PCR assay was developed for the sub clinical detection of both parasites and to assist in future life cycle studies. PCR revealed that the parasite in P. obscurus was detectable in non-pseudotumourous areas of fish that had pseudotumours present in other areas of the body.

Conclusions: The inability to successfully transmit both parasites in this study suggests that either host detachment combined with a period of independent development or an alternate host is required to complete the life cycle for X-cell parasites. Phylogenetic analyses of SSU rDNA confirm a monophyletic grouping for all sequenced X-cell parasites, but do not robustly support their placement within any established protist phylum. Analysis of SSU rDNA from X-cells in Japanese flatfish reveals that the same parasite can infect more than one species of fish.

Show MeSH
Related in: MedlinePlus