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Beth Okamura - One of the best experts on this subject based on the ideXlab platform.
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Myxozoa polypodium a common route to endoparasitism
Trends in Parasitology, 2016Co-Authors: Beth Okamura, Alexander GruhlAbstract:Recent evidence places the problematic Polypodium, a parasite of fish eggs, firmly as sister taxon to Myxozoa within the Cnidaria. This resolution suggests a single route to endoparasitism in Cnidaria, with larval stages of a common ancestor exploiting fish as first hosts. It also enables new interpretations and insights regarding evolutionary transitions associated with endoparasitism.
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Myxozoa + Polypodium: A Common Route to Endoparasitism
Trends in parasitology, 2016Co-Authors: Beth Okamura, Alexander GruhlAbstract:Recent evidence places the problematic Polypodium, a parasite of fish eggs, firmly as sister taxon to Myxozoa within the Cnidaria. This resolution suggests a single route to endoparasitism in Cnidaria, with larval stages of a common ancestor exploiting fish as first hosts. It also enables new interpretations and insights regarding evolutionary transitions associated with endoparasitism.
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Cnidarian Origins of the Myxozoa
Myxozoan Evolution Ecology and Development, 2015Co-Authors: Beth Okamura, Alexander Gruhl, Abigail J. ReftAbstract:Now that we have strong evidence for the phylogenetic placement of Myxozoa within the Cnidaria it is of great interest to explore their evolutionary history. In particular, what cnidarian features may have facilitated the transition to an endoparasitic lifestyle and can we identify a potential cnidarian sister group? In this chapter we summarise evidence for characters linking Myxozoans to cnidarians and identify cnidarian traits that may have promoted endoparasitism including: their diploblastic condition, their capacity for regeneration, transdifferentiation, and dormancy, the production of novel propagative stages, cell-within-cell development, and asexual reproduction. Equating the basic cnidarian life cycle (benthic polyps and planktonic medusae) with the complex Myxozoan life cycle is problematic because of great plasticity in cnidarian development, which can entail the loss of stages and associated transfer of function. The sexual phase of Myxozoans involves the production of isogametes but divergent views on their subsequent fusion lead to questions about whether sexual reproduction involves selfing or outcrossing and if it may result in the development of multicellular chimaeras. The apical structures of Myxozoan polar capsules closely resemble those of medusozoan but not those of anthozoan nematocysts, thus supporting a medusozoan affinity for Myxozoa.
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Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution.
EvoDevo, 2012Co-Authors: Alexander Gruhl, Beth OkamuraAbstract:Background The enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most Myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of Myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other Myxozoans and therefore is of specific significance for such evolutionary considerations.
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development and myogenesis of the vermiform buddenbrockia Myxozoa and implications for cnidarian body plan evolution
Evodevo, 2012Co-Authors: Alexander Gruhl, Beth OkamuraAbstract:Background: The enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most Myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of Myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other Myxozoans and therefore is of specific significance for such evolutionary considerations. Methods: We analyse and describe the development of major body plan features in Buddenbrockia worms using a combination of histology, electron microscopy and confocal microscopy. Results: Early developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function. Conclusions: The polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.
Astrid S. Holzer - One of the best experts on this subject based on the ideXlab platform.
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Genetic Diversity of Serine Protease Inhibitors in Myxozoan (Cnidaria, Myxozoa) Fish Parasites.
Microorganisms, 2020Co-Authors: Edit Eszterbauer, Ivan Fiala, Dóra Sipos, Győző L Kaján, Dóra Szegő, Astrid S. Holzer, Pavla Bartošová-sojkováAbstract:We studied the genetic variability of serine protease inhibitors (serpins) of Myxozoa, microscopic endoparasites of fish. Myxozoans affect the health of both farmed and wild fish populations, causing diseases and mortalities. Despite their global impact, no effective protection exists against these parasites. Serpins were reported as important factors for host invasion and immune evasion, and as promising targets for the development of antiparasitic therapies. For the first time, we identified and aligned serpin sequences from high throughput sequencing datasets of ten Myxozoan species, and analyzed 146 serpins from this parasite group together with those of other taxa phylogenetically, to explore their relationship and origins. High intra- and interspecific variability was detected among the examined serpins. The average sequence identity was 25-30% only. The conserved domains (i.e., motif and signature) showed taxon-level differences. Serpins clustered according to taxonomy rather than to serpin types, and Myxozoan serpins seemed to be highly divergent from that of other taxa. None of them clustered with their closest relative free-living cnidarians. The genetic distinction of Myxozoan serpins further strengthens the idea of an independent origin of Myxozoa, and may indicate novel protein functions potentially related to parasitism in this animal group.
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Selection of suitable reference genes for gene expression studies in myxosporean (Myxozoa, Cnidaria) parasites.
Scientific reports, 2019Co-Authors: Anush Kosakyan, Gema Alama-bermejo, Jerri L. Bartholomew, Edit Eszterbauer, Pavla Bartošová-sojková, Ana Born-torrijos, Radek Sima, Anna Nenarokova, Astrid S. HolzerAbstract:Myxozoans (Cnidaria: Myxozoa) are an extremely diversified group of endoparasites some of which are causative agents of serious diseases in fish. New methods involving gene expression studies have emerged over the last years to better understand and control Myxozoan diseases. Quantitative RT-PCR is the most extensively used approach for gene expression studies. However, the accuracy of the results depends on the normalization of the data to reference genes. We studied the expression of eight commonly used reference genes, adenosylhomocysteinase (AHC1), beta actin (ACTB), eukaryotic translation elongation factor 2 (EF2), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), hypoxanthine-guanine phosphoribosyltransferase 1 (HPRT1), DNA-directed RNA polymerase II (RPB2), 18S ribosomal RNA (18S), 28S ribosomal RNA (28S) across different developmental stages of three Myxozoan species, Sphaerospora molnari, Myxobolus cerebralis and Ceratonova shasta, representing the three major Myxozoan linages from the largest class Myxosporea. The stable reference genes were identified using four algorithms: geNorm, NormFinder, Bestkeeper and ΔCq method. Additionally, we analyzed transcriptomic data from S. molnari proliferative and spore-forming stages to compare the relative amount of expressed transcripts with the most stable reference genes suggested by RT-qPCR. Our results revealed that GAPDH and EF2 are the most uniformly expressed genes across the different developmental stages of the studied Myxozoan species.
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The joint evolution of the Myxozoa and their alternate hosts: A cnidarian recipe for success and vast biodiversity.
Molecular ecology, 2018Co-Authors: Astrid S. Holzer, Pavla Bartošová-sojková, Ana Born-torrijos, Alena Lövy, Ashlie Hartigan, Ivan FialaAbstract:The relationships between parasites and their hosts are intimate, dynamic and complex; the evolution of one is inevitably linked to the other. Despite multiple origins of parasitism in the Cnidaria, only parasites belonging to the Myxozoa are characterized by a complex life cycle, alternating between fish and invertebrate hosts, as well as by high species diversity. This inspired us to examine the history of adaptive radiations in Myxozoans and their hosts by determining the degree of congruence between their phylogenies and by timing the emergence of Myxozoan lineages in relation to their hosts. Recent genomic analyses suggested a common origin of Polypodium hydriforme, a cnidarian parasite of acipenseriform fishes, and the Myxozoa, and proposed fish as original hosts for both sister lineages. We demonstrate that the Myxozoa emerged long before fish populated Earth and that phylogenetic congruence with their invertebrate hosts is evident down to the most basal branches of the tree, indicating bryozoans and annelids as original hosts and challenging previous evolutionary hypotheses. We provide evidence that, following invertebrate invasion, fish hosts were acquired multiple times, leading to parallel cospeciation patterns in all major phylogenetic lineages. We identify the acquisition of vertebrate hosts that facilitate alternative transmission and dispersion strategies as reason for the distinct success of the Myxozoa, and identify massive host specification-linked parasite diversification events. The results of this study transform our understanding of the origins and evolution of parasitism in the most basal metazoan parasites known.
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Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa).
Molecular phylogenetics and evolution, 2013Co-Authors: Pavla Bartošová, Ivan Fiala, Stephen D. Atkinson, Jerri L. Bartholomew, Miloslav Jirků, Martina Cinková, Monica Caffara, Marialetizia Fioravanti, Astrid S. HolzerAbstract:Abstract Myxosporeans (Myxozoa) are eukaryotic parasites, primarily of fish, whose classification is in a state of flux as taxonomists attempt to synthesize the traditional morphology-based system with emerging DNA sequence-based phylogenies. The genus Sphaerospora Thelohan, 1892, which includes pathogenic species that cause significant impacts on fisheries and aquaculture, is one of the most polyphyletic taxa and exemplifies the current challenges facing Myxozoan taxonomists. The type species, S. elegans, clusters within the Sphaerospora sensu stricto clade, members of which share similar tissue tropism and long insertions in their variable rRNA gene regions. However, other morphologically similar sphaerosporids lie in different branches of Myxozoan phylogenetic trees. Herein, we significantly extend taxonomic sampling of sphaerosporids with SSU + LSU rDNA and EF-2 sequence data for 12 taxa including three representatives of the morphologically similar genus Polysporoplasma Sitja-Bobadilla et Alvarez-Pellitero, 1995. These taxa were sampled from different vertebrate host groups, biogeographic realms and environments. Our phylogenetic analyses and statistical tests of single and concatenated datasets revealed Sphaerospora s. s. as a strongly supported monophyletic lineage, that clustered sister to the whole myxosporean clade (freshwater + marine lineages). Generally, Sphaerospora s. s. rDNA sequences (up to 3.7 kb) are the longest of all Myxozoans and indeed metazoans. The sphaerosporid clade has two lineages, which have specific morphological, biological and sequence traits. Lineage A taxa (marine Sphaerospora spp.) have a single binucleate sporoplasm and shorter AT-rich rDNA inserts. Lineage B taxa (freshwater/brackish Sphaerospora spp. + marine/brackish Polysporoplasma spp.) have 2–12 uninucleate sporoplasms and longer GC-rich rDNA inserts. Lineage B has four subclades that correlate with host group and habitat; all Polysporoplasma species, including the type species, cluster together in one of these subclades. We thus suppress the genus Polysporoplasma and the family Polysporoplasmidae and emend the generic diagnosis of the genus Sphaerospora. The combination of morphological, biological and DNA sequence data applied in this study helped to elucidate an important part of the taxonomic puzzle within the phylum Myxozoa.
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3d morphology ultrastructure and development of ceratomyxa puntazzi stages first insights into the mechanisms of motility and budding in the Myxozoa
PLOS ONE, 2012Co-Authors: Gema Alamabermejo, Astrid S. Holzer, James E Bron, Juan Antonio RagaAbstract:Free, amoeboid movement of organisms within media as well as substrate-dependent cellular crawling processes of cells and organisms require an actin cytoskeleton. This system is also involved in the cytokinetic processes of all eukaryotic cells. Myxozoan parasites are known for the disease they cause in economical important fishes. Usually, their pathology is related to rapid proliferation in the host. However, the sequences of their development are still poorly understood, especially with regard to pre-sporogonic proliferation mechanisms. The present work employs light microscopy (LM), electron microscopy (SEM, TEM) and confocal laser scanning microscopy (CLSM) in combination with specific stains (Nile Red, DAPI, Phalloidin), to study the three-dimensional morphology, motility, ultrastructure and cellular composition of Ceratomyxa puntazzi, a Myxozoan inhabiting the bile of the sharpsnout seabream. Our results demonstrate the occurrence of two C. puntazzi developmental cycles in the bile, i.e. pre-sporogonic proliferation including frequent budding as well as sporogony, resulting in the formation of durable spore stages and we provide unique details on the ultrastructure and the developmental sequence of bile inhabiting Myxozoans. The present study describes, for the first time, the cellular components and mechanisms involved in the motility of Myxozoan proliferative stages, and reveals how the same elements are implicated in the processes of budding and cytokinesis in the Myxozoa. We demonstrate that F-actin rich cytoskeletal elements polarize at one end of the parasites and in the filopodia which are rapidly de novo created and re-absorbed, thus facilitating unidirectional parasite motility in the bile. We furthermore discover the Myxozoan mechanism of budding as an active, polarization process of cytokinesis, which is independent from a contractile ring and thus differs from the mechanism, generally observed in eurkaryotic cells. We hereby demonstrate that CLSM is a powerful tool for Myxozoan research with a great potential for exploitation, and we strongly recommend its future use in combination with in vivo stains.
Elizabeth U. Canning - One of the best experts on this subject based on the ideXlab platform.
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Biodiversity and evolution of the Myxozoa
Advances in parasitology, 2004Co-Authors: Elizabeth U. Canning, Beth OkamuraAbstract:Myxozoans (phylum Myxozoa) are metazoan parasites utilizing invertebrate and (mainly) aquatic vertebrate hosts. They have in common with cnidarians the possession of virtually identical, highly complex organelles, namely the polar capsules in Myxozoan spores, serving for attachment to new hosts and the nematocysts in surface epithelia of cnidarians, serving for food capture. Although Myxozoan spores are multicellular, the simple trophic body forms of almost all species, reduced to syncytial plasmodia or single cells, reveal no clues to Myxozoan ancestry or phylogenetic relationships. The Myxozoan genus Buddenbrockia is one of only two known genera belonging to a clade which diverged early in the evolution of the Myxozoa. Today the Myxozoa are represented by two classes, the Myxosporea, containing all the better-known genera, which alternate between fish and annelids, and the Malacosporea, containing Buddenbrockia and Tetracapsuloides, parasitising bryozoans. The latter genus also infects salmonid fish, causing proliferative kidney disease (PKD). The enigmatic Buddenbrockia has retained some of its ancestral features in a body wall of two cell layers and a worm-like shape, maintained by four longitudinally-running muscle blocks, similar to a gutless nematode and suggestive of a bilaterian ancestry. Although some analyses of 18S rDNA sequences tend towards a cnidarian (diploblast) affinity for Myxozoans, the majority of these studies place them within, or sister to, the Bilateria. The latter view is supported by their possession of central class Hox genes, so far considered to be synapomorphic for Bilateria. The simple body form is, therefore, an extreme example of simplification due to parasitism. Various hypotheses for the occurrence of identical complex organelles (nematocysts and polar capsules) in diploblast and triploblast phyla are evaluated: common ancestry, convergent evolution, gene transfer and, especially, endosymbiosis. A theory of the evolution of their digenetic life cycles is proposed, with the invertebrate as primary host and secondary acquisition of the vertebrate host serving for asexual population increase.
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Ultrastructure of Buddenbrockia identifies it as a Myxozoan and verifies the bilaterian origin of the Myxozoa
Parasitology, 2002Co-Authors: Beth Okamura, Alan Curry, Timothy S. Wood, Elizabeth U. CanningAbstract:The phylogenetic affinities of Buddenbrockia, a nematode-like parasite of freshwater bryozoans, have remained unknown since it was first reported in the nineteenth century. The discovery of Buddenbrockia parasitic in Hyalinella punctata in Ohio and Plumatella repens in France has provided material for the first ultrastructural study of this animal. This has revealed the presence of polar capsules, diagnostic Myxozoan features, in the body wall. Other features, which place Buddenbrockia firmly among tetracapsulid Myxozoans in the Class Malacosporea, are the unusual morphology of the polar capsules, the absence of the external tube in capsulogenesis, the body wall with its unusual cell junctions and utilization of freshwater bryozoans as hosts. The ultrastructural study has established the triploblastic organization of Buddenbrockia by confirmation of the presence of an inner layer of cells and 4 sets of longitudinal muscles. Our studies have, thus, simultaneously revealed that Buddenbrockia is a Myxozoan and that the Myxozoans are derived from bilaterians. The latter conclusion resolves the ongoing controversy over the triploblastic versus diploblastic nature of the Myxozoa. Our studies also provide evidence that bryozoans are ancestral hosts for the Myxozoans and that loss of triploblast features has characterized the major radiation of the better known endoparasites of fish and worms in the Class Myxosporea.
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ecology development and pathogenicity of buddenbrockia plumatellae schroder 1910 Myxozoa malacosporea syn tetracapsula bryozoides and establishment of tetracapsuloides n gen for tetracapsula bryosalmonae
Journal of Eukaryotic Microbiology, 2002Co-Authors: Elizabeth U. Canning, Alan Curry, Timothy S. Wood, Sylvie Tops, Beth OkamuraAbstract:Buddenbrockia plumatellae, an enigmatic worm-like Myxozoan, was observed as continuously writhing free and attached 'worms' and as free mature spores in the coelom of the freshwater bryozoans Plumatella fungosa, Hyalinella punctata, and Fredericella sp. 'Worm' numbers could double every three days. 'Worms' and spores could be expelled from colonies by external pressure. Some mature 'worms' exited actively, entraining release of free spores, and gradually ceased movement outside the host. Bryozoans sealed off infected regions of the colony. Infected colonies grew slowly, produced no statoblasts, and eventually regressed and died. Transmission was not achieved and prevalence was low. Electron microscopy of 'worms' revealed a single layer of mural cells on a fibrous basal lamina overlying four longitudinal muscle blocks and an inner sheet of two types of proliferating cells, an organization indicative of the bilaterian ancestry of the Myxozoa. Primary type A cells were attached directly by striated tubules to mural cells at positions between muscle blocks. Secondary type A cells had a secretory function. Type B cells underwent meiosis and subsequently developed to typical malacosporean Myxozoan spores filling the internal cavity of the 'worms'. External tubes were formed during capsulogenesis in 'worms' from Fredericella sp. Tetracapsula bryozoides is synonymised with Buddenbrockia plumatellae and a new genus is proposed for Tetracapsula bryosalmonae.
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Molecular data implicate bryozoans as hosts for PKX (phylum Myxozoa) and identify a clade of bryozoan parasites within the Myxozoa.
Parasitology, 1999Co-Authors: Cort L. Anderson, Elizabeth U. Canning, Beth OkamuraAbstract:Proliferative kidney disease (PKD), a condition associated with high mortality in salmonid fish, represents an abnormal immune response to the presence of an enigmatic Myxozoan, which has been designated simply as PKX organism because its generic and specific status are obscure. Phylogenetic analyses of partial sequences of the 18S rDNA of PKX and of Myxozoan parasites infecting the bryozoans Cristatella mucedo, Pectinatella magnifica and Plumatella rugosa, including the previously named Tetracapsula bryozoides from C. mucedo, showed that these taxa represent a distinct clade that diverged early in the evolution of the Myxozoa before the radiation of the other known Myxozoan genera. A common feature of the Myxozoans in this clade may be the electron-dense sporoplasmosomes with a lucent bar-like structure, which occur in T. bryozoides and PKX but not in the Myxozoans belonging to the established orders Bivalvulida and Multivalvulida. Variation of 0.5-1.1% was found among the PKX 18S rDNA sequences obtained from fish from North America and Europe. The 18S rDNA sequence for T. bryozoides showed that it is a distinct taxon, not closely related to PKX but some sequences from Myxozoans infecting 2 of the bryozoan species were so similar to those of PKX as to be indistinguishable. Other sequences from the new Myxozoans in bryozoans at first appeared distinct from PKX in a maximum likelihood tree but, when analysed further, were also found to be phylogenetically indistinguishable from PKX. We propose that at least some variants of these new Myxozoans from bryozoans are able to infect and multiply in salmonid fish, in which they stimulate the immune reaction and cause PKD but are unable to form mature spores to complete their development.
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A triploblast origin for Myxozoa
Nature, 1998Co-Authors: Cort L. Anderson, Elizabeth U. Canning, Beth OkamuraAbstract:Hox genes, which play key roles in the development of body plans, have been described from a variety of metazoans1. Here we report the presence of Hox class genes that are typical of triploblasts in Myxozoa, formerly a protozoan taxon. This finding confirms Myxozoa's phylogenetic affinity with the Bilateria and reveals an extreme example of parasitic degeneracy.
Jerri L. Bartholomew - One of the best experts on this subject based on the ideXlab platform.
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A comparison of the structure and function of nematocysts in free-living and parasitic cnidarians (Myxozoa).
International journal for parasitology, 2020Co-Authors: Benjamin Americus, Jerri L. Bartholomew, Tamar Lotan, Stephen D. AtkinsonAbstract:Abstract Myxozoans are obligate parasites that have complex life cycles requiring alternate vertebrate and invertebrate hosts, with transmission via microscopic waterborne spores. Unusually for parasites, they belong to the phylum Cnidaria, alongside thousands of free-living corals, sea anemones, jellyfish and hydrozoans. Their cnidarian affinity is affirmed by genetic relatedness and the presence of nematocysts, historically called “polar capsules” in Myxozoan research. Free-living cnidarians utilise this cellular weaponry for defence, predation and adhesion, whereas Myxozoans use it to anchor to their hosts as the first step in infection. Despite the ~650 million years of divergence between free-living cnidarians and Myxozoans, their nematocysts retain many shared morphological and molecular characters. Both are intra-cellular capsules with a single opening, and contain a coiled, evertable tubule. They are composed of unique nematocyst proteins, nematogalectin and minicollagen, and both likely contain an internal matrix of metal cations covalently bound to the anionic polymer poly-gamma glutamate. The rapid dissociation of this matrix and the resulting increase in internal osmotic potential is the driving force behind tubule elongation during discharge. In this review, we compare the structure and function of nematocysts in Myxozoa and free-living Cnidaria, incorporating recent molecular characterizations. We propose that terminology for homologous Myxozoan structures be synonymized with those from other Cnidaria, hence, “polar capsule” as a taxon-specific nematocyst morphotype and “polar filament” as “tubule.” Despite taxonomic divergence, genome reduction and an evolution to parasitism, Myxozoans maintain nematocysts that are structurally and functionally homologous to those of their free-living cnidarian relatives.
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Selection of suitable reference genes for gene expression studies in myxosporean (Myxozoa, Cnidaria) parasites.
Scientific reports, 2019Co-Authors: Anush Kosakyan, Gema Alama-bermejo, Jerri L. Bartholomew, Edit Eszterbauer, Pavla Bartošová-sojková, Ana Born-torrijos, Radek Sima, Anna Nenarokova, Astrid S. HolzerAbstract:Myxozoans (Cnidaria: Myxozoa) are an extremely diversified group of endoparasites some of which are causative agents of serious diseases in fish. New methods involving gene expression studies have emerged over the last years to better understand and control Myxozoan diseases. Quantitative RT-PCR is the most extensively used approach for gene expression studies. However, the accuracy of the results depends on the normalization of the data to reference genes. We studied the expression of eight commonly used reference genes, adenosylhomocysteinase (AHC1), beta actin (ACTB), eukaryotic translation elongation factor 2 (EF2), glyceraldehyde-3-phosphate dehydrogenase (GAPDH), hypoxanthine-guanine phosphoribosyltransferase 1 (HPRT1), DNA-directed RNA polymerase II (RPB2), 18S ribosomal RNA (18S), 28S ribosomal RNA (28S) across different developmental stages of three Myxozoan species, Sphaerospora molnari, Myxobolus cerebralis and Ceratonova shasta, representing the three major Myxozoan linages from the largest class Myxosporea. The stable reference genes were identified using four algorithms: geNorm, NormFinder, Bestkeeper and ΔCq method. Additionally, we analyzed transcriptomic data from S. molnari proliferative and spore-forming stages to compare the relative amount of expressed transcripts with the most stable reference genes suggested by RT-qPCR. Our results revealed that GAPDH and EF2 are the most uniformly expressed genes across the different developmental stages of the studied Myxozoan species.
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Sphaerospora sensu stricto: taxonomy, diversity and evolution of a unique lineage of myxosporeans (Myxozoa).
Molecular phylogenetics and evolution, 2013Co-Authors: Pavla Bartošová, Ivan Fiala, Stephen D. Atkinson, Jerri L. Bartholomew, Miloslav Jirků, Martina Cinková, Monica Caffara, Marialetizia Fioravanti, Astrid S. HolzerAbstract:Abstract Myxosporeans (Myxozoa) are eukaryotic parasites, primarily of fish, whose classification is in a state of flux as taxonomists attempt to synthesize the traditional morphology-based system with emerging DNA sequence-based phylogenies. The genus Sphaerospora Thelohan, 1892, which includes pathogenic species that cause significant impacts on fisheries and aquaculture, is one of the most polyphyletic taxa and exemplifies the current challenges facing Myxozoan taxonomists. The type species, S. elegans, clusters within the Sphaerospora sensu stricto clade, members of which share similar tissue tropism and long insertions in their variable rRNA gene regions. However, other morphologically similar sphaerosporids lie in different branches of Myxozoan phylogenetic trees. Herein, we significantly extend taxonomic sampling of sphaerosporids with SSU + LSU rDNA and EF-2 sequence data for 12 taxa including three representatives of the morphologically similar genus Polysporoplasma Sitja-Bobadilla et Alvarez-Pellitero, 1995. These taxa were sampled from different vertebrate host groups, biogeographic realms and environments. Our phylogenetic analyses and statistical tests of single and concatenated datasets revealed Sphaerospora s. s. as a strongly supported monophyletic lineage, that clustered sister to the whole myxosporean clade (freshwater + marine lineages). Generally, Sphaerospora s. s. rDNA sequences (up to 3.7 kb) are the longest of all Myxozoans and indeed metazoans. The sphaerosporid clade has two lineages, which have specific morphological, biological and sequence traits. Lineage A taxa (marine Sphaerospora spp.) have a single binucleate sporoplasm and shorter AT-rich rDNA inserts. Lineage B taxa (freshwater/brackish Sphaerospora spp. + marine/brackish Polysporoplasma spp.) have 2–12 uninucleate sporoplasms and longer GC-rich rDNA inserts. Lineage B has four subclades that correlate with host group and habitat; all Polysporoplasma species, including the type species, cluster together in one of these subclades. We thus suppress the genus Polysporoplasma and the family Polysporoplasmidae and emend the generic diagnosis of the genus Sphaerospora. The combination of morphological, biological and DNA sequence data applied in this study helped to elucidate an important part of the taxonomic puzzle within the phylum Myxozoa.
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myxidium scripta n sp identified in urinary and biliary tract of louisiana farmed red eared slider turtles trachemys scripta elegans
Diseases of Aquatic Organisms, 2008Co-Authors: John F. Roberts, Lynda Schneider, Christopher M. Whipps, Jerri L. Bartholomew, Elliott R JacobsonAbstract:During a necropsy investigation of a mortality event occurring at a turtle farm in Assumption Parish, Louisiana, spores of a Myxozoan were identified in the renal tubules in 3 of 6, the gall bladder lumen in 2 of 6, and the bile ductule in 1 of 6 red eared slider turtles Trachemys scripta elegans. In total, Myxozoa were identified in 4 of 6 turtles. In 1 turtle, renal tubules contained numer- ous mature spores, had epithelial hyperplasia, granulomatous transformation, compression of adja- cent tubules and interstitial lymphocytic nephritis. The genus of Myxozoan was Myxidium, based on spore morphology in cytological preparations, in histologic section, and by electron microscopy. In cytological preparation the spores had mean dimensions of 18.8 × 5.1 µm and a mean polar capsule dimension of 6.6 × 3.5 µm. Electron microscopy showed renal tubules contained plasmodia with disporoblasts with spores in various stages of maturation. Ultrastructure of mature spores demon- strated a capsule containing 2 asymmetrical overlapping valves and polar capsules containing a polar filament coiled 6 to 8 times and surrounded by a membrane composed of a double layer wall. The small subunit rDNA gene sequence was distinct from all other Myxidium species for which sequences are available. Additionally, this is the first Myxidium species recovered from a North American chelonian to receive genetic analysis. Although T. s. elegans is listed as a host for Myxid- ium chelonarum, this newly described species of Myxidium possessed larger spores with tapered ends; thus, we described it as a new species, Myxidium scripta n. sp. This report documents a clini- cally significant nephropathy and genetic sequence from a Myxidium parasite affecting a freshwater turtle species in North America.
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Myxozoan parasitism in waterfowl
International Journal for Parasitology, 2008Co-Authors: Jerri L. Bartholomew, Sascha L. Hallett, Bruce A Rideout, Michael K Keel, Chris H Gardiner, Stephen D. Atkinson, Linda J. Lowenstine, Michael M. Garner, Justin D. BrownAbstract:Abstract Myxozoans are spore-forming, metazoan parasites common in cold-blooded aquatic vertebrates, especially fishes, with alternate life cycle stages developing in invertebrates. We report nine cases of infection in free-flying native and captive exotic ducks (Anseriformes: Anatidae) from locations across the United States and describe the first Myxozoan in birds, Myxidium anatidum n. sp. We found developmental stages and mature spores in the bile ducts of a Pekin duck (domesticated Anas platyrhynchos ). Spores are lens-shaped in sutural view, slightly sigmoidal in valvular view, with two polar capsules, and each valve cell has 14–16 longitudinal surface ridges. Spore dimensions are 23.1 μm × 10.8 μm × 11.2 μm. Phylogenetic analysis of the ssrRNA gene revealed closest affinity with Myxidium species described from chelonids (tortoises). Our novel finding broadens the definition of the Myxozoa to include birds as hosts and has implications for understanding Myxozoan evolution, and mechanisms of geographical and host range extension. The number of infection records indicates this is not an incidental occurrence, and the detection of such widely dispersed cases suggests more Myxozoans in birds will be encountered with increased surveillance of these hosts for pathogens.
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Myxozoa polypodium a common route to endoparasitism
Trends in Parasitology, 2016Co-Authors: Beth Okamura, Alexander GruhlAbstract:Recent evidence places the problematic Polypodium, a parasite of fish eggs, firmly as sister taxon to Myxozoa within the Cnidaria. This resolution suggests a single route to endoparasitism in Cnidaria, with larval stages of a common ancestor exploiting fish as first hosts. It also enables new interpretations and insights regarding evolutionary transitions associated with endoparasitism.
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Myxozoa + Polypodium: A Common Route to Endoparasitism
Trends in parasitology, 2016Co-Authors: Beth Okamura, Alexander GruhlAbstract:Recent evidence places the problematic Polypodium, a parasite of fish eggs, firmly as sister taxon to Myxozoa within the Cnidaria. This resolution suggests a single route to endoparasitism in Cnidaria, with larval stages of a common ancestor exploiting fish as first hosts. It also enables new interpretations and insights regarding evolutionary transitions associated with endoparasitism.
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Cnidarian Origins of the Myxozoa
Myxozoan Evolution Ecology and Development, 2015Co-Authors: Beth Okamura, Alexander Gruhl, Abigail J. ReftAbstract:Now that we have strong evidence for the phylogenetic placement of Myxozoa within the Cnidaria it is of great interest to explore their evolutionary history. In particular, what cnidarian features may have facilitated the transition to an endoparasitic lifestyle and can we identify a potential cnidarian sister group? In this chapter we summarise evidence for characters linking Myxozoans to cnidarians and identify cnidarian traits that may have promoted endoparasitism including: their diploblastic condition, their capacity for regeneration, transdifferentiation, and dormancy, the production of novel propagative stages, cell-within-cell development, and asexual reproduction. Equating the basic cnidarian life cycle (benthic polyps and planktonic medusae) with the complex Myxozoan life cycle is problematic because of great plasticity in cnidarian development, which can entail the loss of stages and associated transfer of function. The sexual phase of Myxozoans involves the production of isogametes but divergent views on their subsequent fusion lead to questions about whether sexual reproduction involves selfing or outcrossing and if it may result in the development of multicellular chimaeras. The apical structures of Myxozoan polar capsules closely resemble those of medusozoan but not those of anthozoan nematocysts, thus supporting a medusozoan affinity for Myxozoa.
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Development and myogenesis of the vermiform Buddenbrockia (Myxozoa) and implications for cnidarian body plan evolution.
EvoDevo, 2012Co-Authors: Alexander Gruhl, Beth OkamuraAbstract:Background The enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most Myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of Myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other Myxozoans and therefore is of specific significance for such evolutionary considerations.
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development and myogenesis of the vermiform buddenbrockia Myxozoa and implications for cnidarian body plan evolution
Evodevo, 2012Co-Authors: Alexander Gruhl, Beth OkamuraAbstract:Background: The enigmatic wormlike parasite Buddenbrockia plumatellae has recently been shown to belong to the Myxozoa, which are now supported as a clade within Cnidaria. Most Myxozoans are morphologically extremely simplified, lacking major metazoan features such as epithelial tissue layers, gut, nervous system, body axes and gonads. This hinders comparisons to free-living cnidarians and thus an understanding of Myxozoan evolution and identification of their cnidarian sister group. However, B. plumatellae is less simplified than other Myxozoans and therefore is of specific significance for such evolutionary considerations. Methods: We analyse and describe the development of major body plan features in Buddenbrockia worms using a combination of histology, electron microscopy and confocal microscopy. Results: Early developmental stages develop a primary body axis that shows a polarity, which is manifested as a gradient of tissue development, enabling distinction between the two worm tips. This polarity is maintained in adult worms, which, in addition, often develop a pore at the distal tip. The musculature comprises tetraradially arranged longitudinal muscle blocks consisting of independent myocytes embedded in the extracellular matrix between inner and outer epithelial tissue layers. The muscle fibres are obliquely oriented and in fully grown worms consistently form an angle of 12° with respect to the longitudinal axis of the worm in each muscle block and hence confer chirality. Connecting cells form a link between each muscle block and constitute four rows of cells that run in single file along the length of the worm. These connecting cells are remnants of the inner epithelial tissue layer and are anchored to the extracellular matrix. They are likely to have a biomechanical function. Conclusions: The polarised primary body axis represents an ancient feature present in the last common ancestor of Cnidaria and Bilateria. The tetraradial arrangement of musculature is consistent with a medusozoan affinity for Myxozoa. However, the chiral pattern of muscle fibre orientation is apparently novel within Cnidaria and could thus be a specific adaptation. The presence of independent myocytes instead of Cnidaria-like epitheliomuscular cells can be interpreted as further support for the presence of mesoderm in cnidarians, or it may represent convergent evolution to a bilaterian condition.
