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The Molecular Mechanisms Employed by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) from Invasion through Sporulation for Successful Proliferation in Its Fish Host.

ABSTRACT: Myxozoa is a unique group of obligate endoparasites in the phylum Cnidaria that can cause emerging diseases in wild and cultured fish populations. Recently, we identified a new myxozoan species, Myxobolus bejeranoi, which infects the gills of cultured tilapia while suppressing host immunity. To uncover the molecular mechanisms underlying this successful parasitic strategy, we conducted transcriptomics analysis of M. bejeranoi throughout the infection. Our results show that histones, which are essential for accelerated cell division, are highly expressed even one day after invasion. As the infection progressed, conserved parasitic genes that are known to modulate the host immune reaction in different parasitic taxa were upregulated. These genes included energy-related glycolytic enzymes, as well as calreticulin, proteases, and miRNA biogenesis proteins. Interestingly, myxozoan calreticulin formed a distinct phylogenetic clade apart from other cnidarians, suggesting a possible function in parasite pathogenesis. Sporogenesis was in its final stages 20 days post-exposure, as spore-specific markers were highly expressed. Lastly, we provide the first catalog of transcription factors in a Myxozoa species, which is minimized compared to free-living cnidarians and is dominated by homeodomain types. Overall, these molecular insights into myxozoan infection support the concept that parasitic strategies are a result of convergent evolution.

SUBMITTER: Maor-Landaw K

PROVIDER: S-EPMC10454682 | biostudies-literature | 2023 Aug

REPOSITORIES: biostudies-literature

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The Molecular Mechanisms Employed by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) from Invasion through Sporulation for Successful Proliferation in Its Fish Host.

Maor-Landaw Keren K Avidor Itamar I Rostowsky Nadav N Salti Barbara B Smirnov Margarita M Ofek-Lalzar Maya M Levin Liron L Brekhman Vera V Lotan Tamar T

International journal of molecular sciences 20230815 16

Myxozoa is a unique group of obligate endoparasites in the phylum Cnidaria that can cause emerging diseases in wild and cultured fish populations. Recently, we identified a new myxozoan species, Myxobolus bejeranoi, which infects the gills of cultured tilapia while suppressing host immunity. To uncover the molecular mechanisms underlying this successful parasitic strategy, we conducted transcriptomics analysis of M. bejeranoi throughout the infection. Our results show that histones ...[more]

PMID: 37629003

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Project description:BACKGROUND:Myxozoa are extremely diverse microscopic parasites belonging to the Cnidaria. Their life-cycles alternate between vertebrate and invertebrate hosts, predominantly in aquatic habitats. Members of the phylogenetically well-defined Sphaerospora (sensu stricto) clade predominantly infect the urinary system of marine and freshwater fishes and amphibians. Sphaerosporids are extraordinary due to their extremely long and unique insertions in the variable regions of their 18S and 28S rDNA genes and due to the formation of motile proliferative stages in the hosts' blood. To date, DNA sequences of only 19 species have been obtained and information on the patterns responsible for their phylogenetic clustering is limited. METHODS:We screened 549 fish kidney samples from fish of various geographical locations, mainly in central Europe, to investigate sphaerosporid biodiversity microscopically and by 18S rDNA sequences. We performed multiple phylogenetic analyses to explore phylogenetic relationships and evolutionary trends within the Sphaerospora (s.s.) clade, by matching host and habitat features to the resultant 18S rDNA trees. The apparent co-clustering of species from related fish hosts inspired us to further investigate host-parasite co-diversification, using tree-based (CoRE-PA) and distance-based (ParaFit) methods. RESULTS:Our study considerably increased the number of 18S rDNA sequence data for Sphaerospora (s.s.) by sequencing 17 new taxa. Eight new species are described and one species (Sphaerospora diminuta Li & Desser, 1985) is redescribed, accompanied by sufficient morphological data. Phylogenetic analyses showed that sphaerosporids cluster according to their vertebrate host order and habitat, but not according to geography. Cophylogenetic analyses revealed a significant congruence between the phylogenetic trees of sphaerosporids and of their vertebrate hosts and identified Cypriniformes as a host group of multiple parasite lineages and with high parasite diversity. CONCLUSIONS:This study significantly contributed to our knowledge of the biodiversity and evolutionary history of the members of the Sphaerospora (s.s.) clade. The presence of two separate phylogenetic lineages likely indicates independent historical host entries, and the remarkable overlap of the larger clade with vertebrate phylogeny suggests important coevolutionary adaptations. Hyperdiversification of sphaerosporids in cypriniform hosts, which have undergone considerable radiations themselves, points to host-driven diversification.

Project description:Here, we investigated the early development of two closely related myxozoan parasites, the highly pathogenic Myxobolus cerebralis, the causative agent of the whirling disease in salmonids, and Myxobolus pseudodispar, a common, non-pathogenic parasite of cyprinids. The aim of our study was to examine under in vivo laboratory conditions whether fish blood is involved in the intrapiscine development of the two parasite species and investigate if there is dissimilarity between the parasite infection intensity in blood and if it varies in terms of host susceptibility and parasite pathogenicity. Highly susceptible, less susceptible and non-susceptible hosts were involved. Blood samples were taken 1 day, 1 week and 1 month post exposure to M. cerebralis and M. pseudodispar, respectively. The prevalence and infection intensity was estimated by parasite-specific quantitative real-time PCR. Although previous findings assumed that M. cerebralis might escape from host immune system by migrating via peripheral nerves, our experimental results demonstrated that M. cerebralis is present in blood during the early stage of intrapiscine development. For the non-pathogenic M. pseudodispar, the highest infection prevalence was found in the original host, common roach Rutilus rutilus, whereas the highest infection intensity was detected in rudd Scardinius erythrophthalmus, a "dead-end" host of the parasite. The presence of M. pseudodispar developmental stages in the blood of both susceptible and non-susceptible cyprinids suggests that the susceptibility differences remain hidden during the early stage of infection. Our findings supply further evidence that host specificity is not determined during the early, intrapiscine development involving the vascular system. Furthermore, we found remarkable differences in the infection dynamics of the two parasite species examined, possibly due to their distinct pathogenicity or variations in adaptive capabilities to immune components in host blood.

Dataset Information

The Molecular Mechanisms Employed by the Parasite Myxobolus bejeranoi (Cnidaria: Myxozoa) from Invasion through Sporulation for Successful Proliferation in Its Fish Host.

Publications

The Molecular Mechanisms Employed by the Parasite <i>Myxobolus bejeranoi</i> (Cnidaria: Myxozoa) from Invasion through Sporulation for Successful Proliferation in Its Fish Host.

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