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  1. X-cell parasites in the European dab Limanda limanda are related to other X-cell organisms: a discussion on the potential identity of this new group of parasites
    Freeman MA
    Parasitology, 2009 Aug;136(9):967-80.
    PMID: 19549352 DOI: 10.1017/S0031182009006507
    Unusual tumour-like pathologies caused by mysterious cells termed 'X-cells' have been reported from numerous fish groups worldwide. After nearly 100 years of research, the tumour-like growths have recently been shown to be caused by a protozoan parasite. In the present study, histopathology and small subunit ribosomal DNA (SSU rDNA) sequences are used to assess whether the X-cell parasite infecting Atlantic dab Limanda limanda L. is distinct from the X-cell parasite infecting Japanese flounder and goby, and to determine their systematic position within the protists. SSU rDNA from Scottish dab was 89.3% and 86.7% similar to Japanese X-cell sequences from flounder and goby respectively, indicating that the parasite infecting dab in the Atlantic is distinct from the Pacific species. Histological studies revealed significant gill pathology and demonstrated the precise location of the parasites within the gill tissues using specific in situ hybridization probes. Phylogenetic analyses showed that the X-cell parasites from Scotland and Japan form a monophyletic group within the Myzozoa, and are basal alveolates. However, ultrastructure of X-cells from dab fails to confirm this systematic placement.
  2. Fulltext Negative effects of Kudoa islandica n. sp. (Myxosporea: Kudoidae) on aquaculture and wild fisheries in Iceland
    Kristmundsson A, Freeman MA
    Int J Parasitol Parasites Wildl, 2014 Aug;3(2):135-46.
    PMID: 25161912 DOI: 10.1016/j.ijppaw.2014.06.001
    In the early 2000s, experimental rearing of spotted wolffish, Anarhichas minor, was started in Iceland. Health surveillance, carried out at regular intervals during the rearing period, revealed persistent and highly prevalent Kudoa infections of fish muscles which caused great financial losses due to post mortem myoliquefaction. In addition, during the traditional process of drying and smoking wild Atlantic lumpfish, Cyclopterus lumpus, the muscles from some fish almost completely disappear and the fish have to be discarded. To describe the etiological agent responsible for these conditions, spotted wolffish, Atlantic wolffish Anarhichas lupus, northern wolffish Anarhichas denticulatus and Atlantic lumpfish were caught off the Icelandic coast and examined for the presence of Kudoa. We describe a novel myxosporean, Kudoa islandica n. sp., using morphological and molecular data, and show with histopathology that it causes extensive myoliquefaction in three different wild fish hosts, which all are commercially valuable species in Iceland. Although some spore dimensions varied significantly between fish species, the molecular analyses showed that the same parasite was responsible for infection in all fish. The northern wolffish was not found to be infected. Although robustly placed in the Kudoa clade in phylogenetic analyses, K. islandica was phylogenetically distinct from other kudoids. A single myxosporean, K. islandica, is responsible for the infections in the somatic muscles of lumpfish and wolffish, causing extensive post mortem myoliquefaction. This myxosporean is likely to infect other fish species and it is important to study its life cycle in order to evaluate any threat to salmonid culture via the use of lumpfish as a biocontrol for sea lice.
  3. Fulltext Original observations of Desmozoon lepeophtherii, a microsporidian hyperparasite infecting the salmon louse Lepeophtheirus salmonis, and its subsequent detection by other researchers
    Freeman MA, Sommerville C
    Parasit Vectors, 2011;4:231.
    PMID: 22166354 DOI: 10.1186/1756-3305-4-231
    A microsporidian hyperparasite, Desmozoon lepeophtherii, of the parasitic copepod Lepeophtheirus salmonis (salmon louse), infecting farmed Atlantic salmon (Salmo salar), was first discovered in the west of Scotland in 2000. Heavily infected salmon lice are easily recognised as they have large opaque inclusions distributed throughout the body. The prevalence of salmon lice with visible signs of microsporidiosis can be up to 10% of the population from certain farm sites. The microsporidian was also isolated from the host Atlantic salmon suggesting it may have a two host life cycle. The authors believe that the infection in immunocompetent salmon may be latent, becoming acute during periods of infection with another pathogen or during sexual maturation. Since its first discovery in Scotland, Desmozoon lepeophtherii has been subsequently reported from Norway, and more recently from the Pacific coast of North America.
  4. Variation in the small subunit ribosomal DNA confirms that Udonella (Monogenea: Udonellidae) is a species-rich group
    Freeman MA, Ogawa K
    Int J Parasitol, 2010 Feb;40(2):255-64.
    PMID: 19715695 DOI: 10.1016/j.ijpara.2009.08.006
    Numerous global reports of the species Udonella caligorum, currently thought to be a species complex, suggests that the group may be species-rich. Herein we describe Udonella fugu n. sp., previously described as U. caligorum, found on the parasitic copepod Pseudocaligus fugu infecting Takifugu spp. from Japan. Using morphological data U. fugu can be distinguished from the current valid species by at least one of the traditionally used characters in udonellid taxonomy, and phylogenetic analyses of ssrDNA sequence data for U. fugu and other udonellids confirm that U. fugu forms a distinct clade from other udonellids including U. caligorum. Variable regions in the ssrDNA demonstrated a range of between 2.75 and 5.5% difference between currently recognized species of Udonella. These differences in ssrDNA sequences are phylogenetically useful when distinguishing between morphologically similar udonellids and can be used in conjunction with other data (morphology, phylogeography and fish host) to help clarify udonellid systematics. Udonella fugu was also found to cause significant damage to farmed tiger puffers through their feeding activities. Individual skin lesions were round in shape but merged with adjoining lesions to form more extensive lacerations. In some of the specimens from P. fugu infecting Takifugu niphobles, the protozoan ciliate Trichodina was found on the udonellid body surface and in their intestinal contents. We conclude that the udonellids are a more species-rich group than currently recognized, that early descriptions of new species may have been synonymized with U. caligorum in error and that the frequent global reports of U. caligorum may actually represent new species. This has led to a wide range of morphological descriptions for U. caligorum, blurring the usefulness of morphological data for the group.
  5. Fulltext Studies of Myxidium giardi Cépède, 1906 infections in Icelandic eels identifies a genetically diverse clade of myxosporeans that represents the Paramyxidium n. g. (Myxosporea: Myxidiidae)
    Freeman MA, Kristmundsson Á
    Parasit Vectors, 2018 Oct 22;11(1):551.
    PMID: 30348210 DOI: 10.1186/s13071-018-3087-y
    BACKGROUND: The myxosporean Myxidium giardi Cépède, 1906 was described infecting the kidney of the European eel, Anguilla anguilla (L.), having spindle-shaped myxospores and terminal sub-spherical polar capsules. Since then, numerous anguillid eels globally have been documented to have similar Myxidium infections. Many of these have been identified using the morphological features of myxospores or by the location of infection in the host, and some have been subsequently synonymised with M. giardi. Therefore, it is not clear whether M. giardi is a widely distributed parasite, infecting numerous species of eels, in multiple organs, or whether some infections represent other, morphologically similar but different species of myxosporeans. The aim of the present study was to assess the status of M. giardi infections in Icelandic eels, and related fish hosts in Malaysia and to use spore morphology and molecular techniques to evaluate the diversity of myxosporeans present.

    RESULTS: The morphologies of the myxospores from Icelandic eels were very similar but the overall dimensions were significantly different from the various tissue locations. Myxospores from the kidney of the Malaysian tarpon, Megalops cyprinoides (Broussonet), were noticeably smaller. However, the SSU rDNA sequences from the different tissues locations in eels, were all very distinct, with percentage similarities ranging from 92.93% to as low as 89.8%, with the sequence from Malaysia being even more dissimilar. Molecular phylogenies consistently placed these sequences together in a clade that we refer to as the Paramyxidium clade that is strongly associated with the Myxidium clade (sensu stricto). We erect the genus Paramyxidium n. g. (Myxidiidae) to accommodate these histozoic taxa, and transfer Myxidium giardi as Paramyxidium giardi Cépède, 1906 n. comb. as the type-species.

    CONCLUSIONS: There is not a single species of Myxidium (M. giardi) causing systemic infections in eels in Iceland. There are three species, confirmed with a robust phylogeny, one of which represents Paramyxidium giardi n. comb. Additional species probably exist that infect different tissues in the eel and the site of infection in the host fish is an important diagnostic feature for this group (Paramyxidium n. g. clade). Myxospore morphology is generally conserved in the Paramyxidium clade, although actual spore dimensions can vary between some species. Paramyxidium spp. are currently only known to infect fishes from the Elopomorpha.

  6. Fulltext Histozoic myxosporeans infecting the stomach wall of elopiform fishes represent a novel lineage, the Gastromyxidae
    Freeman MA, Kristmundsson Á
    Parasit Vectors, 2015;8:517.
    PMID: 26453151 DOI: 10.1186/s13071-015-1140-7
    Traditional studies on myxosporeans have used myxospore morphology as the main criterion for identification and taxonomic classification, and it remains important as the fundamental diagnostic feature used to confirm myxosporean infections in fish and other vertebrate taxa. However, its use as the primary feature in systematics has led to numerous genera becoming polyphyletic in subsequent molecular phylogenetic analyses. It is now known that other features, such as the site and type of infection, can offer a higher degree of congruence with molecular data, albeit with its own inconsistencies, than basic myxospore morphology can reliably provide.
  7. Fulltext Myxosporean hyperparasites of gill monogeneans are basal to the multivalvulida
    Freeman MA, Shinn AP
    Parasit Vectors, 2011;4:220.
    PMID: 22115202 DOI: 10.1186/1756-3305-4-220
    Myxosporeans are known from aquatic annelids but parasitism of platyhelminths by myxosporeans has not been widely reported. Hyperparasitism of gill monogeneans by Myxidium giardi has been reported from the European eel and Myxidium-like hyperparasites have also been observed during studies of gill monogeneans from Malaysia and Japan.The present study aimed to collect new hyperparasite material from Malaysia for morphological and molecular descriptions. In addition, PCR screening of host fish was undertaken to determine whether they are also hosts for the myxosporean.
  8. Fulltext Is an Apicomplexan Parasite Responsible for the Collapse of the Iceland Scallop (Chlamys islandica) Stock?
    Kristmundsson Á, Erlingsdóttir Á, Freeman MA
    PLoS One, 2015;10(12):e0144685.
    PMID: 26684810 DOI: 10.1371/journal.pone.0144685
    Due to the total and unexpected collapse of the Iceland scallop, Chlamys islandica, stocks around Iceland during the 2000s, a commercial fishing ban has been imposed on this valuable resource since 2003. Following the initial identification of an apicomplexan parasite in the scallops, a long-term surveillance program was established to evaluate the effect of the parasite on the population. The infections were highly prevalent in all shell sizes throughout the study. However, the parasite only impacts mature scallops where they cause severe macroscopic changes, characterized by an extensively diminished and abnormally coloured adductor muscle. A highly significant relationship was observed between infection intensity and gonad and adductor muscle indices. The first four years of the study, were characterized by high infection intensity and very poor condition of the adductor muscle and gonads, whilst during subsequent years, infections gradually decreased and the condition of the scallops improved. Histopathological changes were restricted to the presence of apicomplexan zoites which were widely distributed, causing varying degrees of pathology in all organs. In heavy infections, muscular and connective tissues were totally necrotized, destroying significant parts of numerous organs, especially the adductor muscle, digestive gland and gonads. The progression of the disease was in good synchrony with the mortality rates and the subsequent decline observed in the scallop stock and recruitment indices. Our findings strongly suggest that the apicomplexan parasite played a major role in the collapse of the Iceland scallop stock in Breidafjordur. In addition to causing mortality, the infections significantly impact gonad development which contributes further to the collapse of the stock in the form of lower larval recruitment. Furthermore, compelling evidence exists that this apicomplexan pathogen is causing serious disease outbreaks in other scallop populations. Similar abnormal adductor muscles and the parasite itself have been identified or observed in association with other mass mortality events in several different scallop species and commercial stocks in the northern hemisphere.
  9. Fulltext Occurrence and molecular identification of Anisakis Dujardin, 1845 from marine fish in southern Makassar Strait, Indonesia
    Anshary H, Sriwulan, Freeman MA, Ogawa K
    Korean J Parasitol, 2014 Feb;52(1):9-19.
    PMID: 24623876 DOI: 10.3347/kjp.2014.52.1.9
    Anisakis spp. (Nematoda: Anisakidae) parasitize a wide range of marine animals, mammals serving as the definitive host and different fish species as intermediate or paratenic hosts. In this study, 18 fish species were investigated for Anisakis infection. Katsuwonus pelamis, Euthynnus affinis, Caranx sp., and Auxis thazard were infected with high prevalence of Anisakis type I, while Cephalopholis cyanostigma and Rastrelliger kanagurta revealed low prevalence. The mean intensity of Anisakis larvae in K. pelamis and A. thazard was 49.7 and 5.6, respectively. A total of 73 Anisakis type I larvae collected from K. pelamis and A. thazard were all identified as Anisakis typica by PCR-RFLP analysis. Five specimens of Anisakis from K. pelamis and 15 specimens from A. thazard were sequenced using ITS1-5.8S-ITS2 region and 6 specimens from A. thazard and 4 specimens from K. pelamis were sequenced in mtDNA cox2 region. Alignments of the samples in the ITS region showed 2 patterns of nucleotides. The first pattern (genotype) of Anisakis from A. thazard had 100% similarity with adult A. typica from dolphins from USA, whereas the second genotype from A. thazard and K. pelamis had 4 base pairs different in ITS1 region with adult A. typica from USA. In the mtDNA cox2 regions, Anisakis type I specimens from A. thazard and K. pelamis showed similarity range from 94% to 99% with A. typica AB517571/DQ116427. The difference of 4 bp nucleotides in ITS1 regions and divergence into 2 subgroups in mtDNA cox2 indicating the existence of A. typica sibling species in the Makassar Strait.
  10. Fulltext Multiple gene analyses of caligid copepods indicate that the reduction of a thoracic appendage in Pseudocaligus represents convergent evolution
    Freeman MA, Anshary H, Ogawa K
    Parasit Vectors, 2013;6(1):336.
    PMID: 24286135 DOI: 10.1186/1756-3305-6-336
    The Caligidae is a family of parasitic copepods containing over 30 recognised genera. They are commercially important parasites as they cause disease in numerous finfish aquaculture facilities globally. Morphological features are used to distinguish between the genera and Pseudocaligus has traditionally been differentiated from Caligus solely by the presence of a much reduced form of the fourth thoracic leg. Currently there are numerous DNA sequences available for Caligus spp. but only the type species, Pseudocaligus brevipedis, has molecular data available, so systematic studies using molecular phylogenetic analyses have been limited.
  11. Spraguea (Microsporida: Spraguidae) infections in the nervous system of the Japanese anglerfish, Lophius litulon (Jordan), with comments on transmission routes and host pathology
    Freeman MA, Yokoyama H, Osada A, Yoshida T, Yamanobe A, Ogawa K
    J Fish Dis, 2011 Jun;34(6):445-52.
    PMID: 21545438 DOI: 10.1111/j.1365-2761.2011.01255.x
    Anglerfish from the genus Lophius are a globally important commercial fishery. The microsporidian Spraguea infects the nervous system of these fish resulting in the formation of large, visible parasitic xenomas. Lophius litulon from Japan were investigated to evaluate the intensity and distribution of Spraguea xenomas throughout the nervous system and to assess pathogenicity to the host and possible transmission routes of the parasite. Spraguea infections in L. litulon had a high prevalence; all fish over 403 mm in standard length being infected, with larger fish usually more heavily infected than smaller fish. Seventy percent of all fish examined had some gross visible sign of infection. The initial site of development is the supramedullary cells on the dorsal surface of the medulla oblongata, where all infected fish have parasitic xenomas. As the disease progresses, a number of secondary sites typically become infected such as the spinal, trigeminal and vagus nerves. Fish with infection in the vagus nerve bundles often have simultaneous sites of infection, in particular the spinal nerves and along the ventral nerve towards the urinary bladder. Advanced vagus nerve infections sometimes form xenomas adjacent to kidney tissue. Spraguea DNA was amplified from the contents of the urinary bladders of two fish, suggesting that microsporidian spores may be excreted in the urine. We conclude that supramedullary cells on the hindbrain are the primary site of infection, which is probably initiated at the cutaneous mucous glands where supramedullary cells are known to extend their peripheral axons. The prevalence of Spraguea infections in L. litulon was very high, and infections often extremely heavy; however, no associated pathogenicity was observed, and heavily infected fish were otherwise normal.
  12. Fulltext Nucleospora cyclopteri n. sp., an intranuclear microsporidian infecting wild lumpfish, Cyclopterus lumpus L., in Icelandic waters
    Freeman MA, Kasper JM, Kristmundsson Á
    Parasit Vectors, 2013;6:49.
    PMID: 23445616 DOI: 10.1186/1756-3305-6-49
    Commercial fisheries of lumpfish Cyclopterus lumpus have been carried out in Iceland for centuries. Traditionally the most valuable part is the eggs which are harvested for use as a caviar substitute.Previously reported parasitic infections from lumpfish include an undescribed intranuclear microsporidian associated with abnormal kidneys and mortalities in captive lumpfish in Canada. During Icelandic lumpfish fisheries in spring 2011, extensive enlargements to the kidneys were observed in some fish during processing. The aim of this study was to identify the pathogen responsible for these abnormalities.
  13. Fulltext A novel histozoic myxosporean, Enteromyxum caesio n. sp., infecting the redbelly yellowtail fusilier, Caesio cuning, with the creation of the Enteromyxidae n. fam., to formally accommodate this commercially important genus
    Freeman MA, Yanagida T, Kristmundsson À
    PeerJ, 2020;8:e9529.
    PMID: 32742799 DOI: 10.7717/peerj.9529
    Gastrointestinal myxosporean parasites from the genus Enteromyxum are known to cause severe disease, resulting in high mortalities in numerous species of cultured marine fishes globally. Originally described as Myxidium spp., they were transferred to a new genus, Enteromyxum, to emphasize their novel characteristics. Their retention in the family Myxidiidae at the time was warranted, but more comprehensive phylogenetic analyses have since demonstrated the need for a new family for these parasites. We discovered a novel Enteromyxum in wild fish from Malaysia and herein describe the fourth species in the genus and erect a new family, the Enteromyxidae n. fam., to accommodate them. Enteromyxum caesio n. sp. is described infecting the tissues of the stomach in the redbelly yellowtail fusilier, Caesio cuning, from Malaysia. The new species is distinct from all others in the genus, as the myxospores although morphologically similar, are significantly smaller in size. Furthermore, small subunit ribosomal DNA sequence data reveal that E. caesio is <84% similar to others in the genus, but collectively they form a robust and discrete clade, the Enteromyxidae n. fam., which is placed as a sister taxon to other histozoic marine myxosporeans. In addition, we describe, using transmission electron microscopy, the epicellular stages of Enteromyxum fugu and show a scanning electron micrograph of a mature myxospore of E. caesio detailing the otherwise indistinct sutural line, features of the polar capsules and spore valve ridges. The Enteromyxidae n. fam. is a commercially important group of parasites infecting the gastrointestinal tract of marine fishes and the histozoic species can cause the disease enteromyxosis in intensive finfish aquaculture facilities. Epicellular and sloughed histozoic stages are responsible for fish-to-fish transmission in net pen aquaculture systems but actinospores from an annelid host are thought to be necessary for transmission to fish in the wild.
  14. Fulltext 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, et al.
    Parasit Vectors, 2011;4:15.
    PMID: 21299903 DOI: 10.1186/1756-3305-4-15
    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.
  15. Zoothamnium duplicatum infestation of cultured horseshoe crabs (Limulus polyphemus)
    Shinn AP, Mühlhölzl AP, Coates CJ, Metochis C, Freeman MA
    J Invertebr Pathol, 2015 Feb;125:81-6.
    PMID: 25499897 DOI: 10.1016/j.jip.2014.12.002
    An outbreak of the sessile peritrich Zoothamnium duplicatum in a pilot, commercial-scale Limulus polyphemus hatchery resulted in the loss of ∼96% (40,000) second/third instar larvae over a 61day period. peritrich growth was heavy, leading to mechanical obstruction of the gills and physical damage. The peritrichs were controlled without resultant loss of juvenile crabs by administering 10ppm chlorine in freshwater for 1h and the addition of aquarium grade sand; a medium into which the crabs could burrow and facilitate cleaning of the carapace. Peritrich identity was confirmed from a partial SSU rDNA contiguous sequence of 1343bp (99.7% similarity to Z. duplicatum).
  16. Evolutionary origin of Ceratonova shasta and phylogeny of the marine myxosporean lineage
    Fiala I, Hlavničková M, Kodádková A, Freeman MA, Bartošová-Sojková P, Atkinson SD
    Mol Phylogenet Evol, 2015 May;86:75-89.
    PMID: 25797924 DOI: 10.1016/j.ympev.2015.03.004
    In order to clarify the phylogenetic relationships among the main marine myxosporean clades including newly established Ceratonova clade and scrutinizing their evolutionary origins, we performed large-scale phylogenetic analysis of all myxosporean species from the marine myxosporean lineage based on three gene analyses and statistical topology tests. Furthermore, we obtained new molecular data for Ceratonova shasta, C. gasterostea, eight Ceratomyxa species and one Myxodavisia species. We described five new species: Ceratomyxa ayami n. sp., C. leatherjacketi n. sp., C. synaphobranchi n. sp., C. verudaensis n. sp. and Myxodavisia bulani n. sp.; two of these formed a new, basal Ceratomyxa subclade. We identified that the Ceratomyxa clade is basal to all other marine myxosporean lineages, and Kudoa with Enteromyxum are the most recently branching clades. Topologies were least stable at the nodes connecting the marine urinary clade, the marine gall bladder clade and the Ceratonova clade. Bayesian inference analysis of SSU rDNA and the statistical tree topology tests suggested that Ceratonova is closely related to the Enteromyxum and Kudoa clades, which represent a large group of histozoic species. A close relationship between Ceratomyxa and Ceratonova was not supported, despite their similar myxospore morphologies. Overall, the site of sporulation in the vertebrate host is a more accurate predictor of phylogenetic relationships than the morphology of the myxospore.
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