The Myxozoa comprise over 2,000 species of microscopic obligate parasites that use both invertebrate and vertebrate hosts as part of their life cycle. Although the evolutionary origin of myxozoans has been elusive, a close relationship with cnidarians, a group that includes corals, sea anemones, jellyfish, and hydroids, is supported by some phylogenetic studies and the observation that the distinctive myxozoan structure, the polar capsule, is remarkably similar to the stinging structures (nematocysts) in cnidarians. To gain insight into the extreme evolutionary transition from a free-living cnidarian to a microscopic endoparasite, we analyzed genomic and transcriptomic assemblies from two distantly related myxozoan species, Kudoa iwatai and Myxobolus cerebralis, and compared these to the transcriptome and genome of the less reduced cnidarian parasite, Polypodium hydriforme. A phylogenomic analysis, using for the first time to our knowledge, a taxonomic sampling that represents the breadth of myxozoan diversity, including four newly generated myxozoan assemblies, confirms that myxozoans are cnidarians and are a sister taxon to P. hydriforme. Estimations of genome size reveal that myxozoans have one of the smallest reported animal genomes. Gene enrichment analyses show depletion of expressed genes in categories related to development, cell differentiation, and cell-cell communication. In addition, a search for candidate genes indicates that myxozoans lack key elements of signaling pathways and transcriptional factors important for multicellular development. Our results suggest that the degeneration of the myxozoan body plan from a free-living cnidarian to a microscopic parasitic cnidarian was accompanied by extreme reduction in genome size and gene content.Myxozoa | Cnidaria | Polypodium | parasite | genome evolution
ABSTRACT. F~sh-to-fish transmission of the marine myxosporean Myxidium lee; was experinlentally demonstrated in sea bream Sparus aurata L. A group of specif~c-pathogen-free (SPF) fish of -11 g each were placed in a wire-mesh cage immersed In a tank holding infected fish. A second group was placed in a tank receiving water discharged from another tank holding diseased fish. After 9 wk, the fish were sacrificed and 12 of the 38 (31.6%) test fish from the mesh cage were found to harbor trophozoites, sporoblasts and spores in the posterior gut epithelium, as was readily diagnosed by standard paraffin histology. Of the fish exposed to water discharge, 10 out of 30 (33.3%) showed similar infection. None of the fish examined displayed any proliferative stages of the parasites in the blood, spleen, kidney, liver or gill samples. All of 100 control fish examined remained uninfected. A third group of SPF fish was fed once daily for 7 d on pieces of freshly dissected M. leei-infected gut, after which the fish were maintained on a commercial pellet diet for a further 4 wk. Control f~s h in this experlrnent were fed only commercial pellets for 5 wk. The fish were sacrificed after 5 wk, and 4 out of 30 test fish (13 %) were found to be infected. All control fish remained uninfected. Examination of the water sampled from all tanks in which infected fish were held revealed presence of exfoliated gut tissue and mucus casts containing trophozoites, sporoblasts and spores of M. leei. Examination of existing potential intermediate hosts yielded definitively negative results for actinosporeans. It is suggested that M. lee1 is transmitted between fish by ingestion of excretions from infected fish. The results reveal that sharing facilities with diseased fish as well as exposure to contaminated water is a route for parasite transmission. In general contrast to the freshwater myxosporeans studied to date, the present study of a marine species provides evidence that d~rect transmission can take place without need for actinosporean developnlent in an alternate (oligochaete) host. It is suggested that this may be a model for the development of other marine myxosporeans as well.
BackgroundMyxozoa are a diverse group of metazoan parasites with a very simple organization, which has for decades eluded their evolutionary origin. Their most prominent and characteristic feature is the polar capsule: a complex intracellular structure of the myxozoan spore, which plays a role in host infection. Striking morphological similarities have been found between myxozoan polar capsules and nematocysts, the stinging structures of cnidarians (corals, sea anemones and jellyfish) leading to the suggestion that Myxozoa and Cnidaria share a more recent common ancestry. This hypothesis has recently been supported by phylogenomic evidence and by the identification of a nematocyst specific minicollagen gene in the myxozoan Tetracapsuloides bryosalmonae. Here we searched genomes and transcriptomes of several myxozoan taxa for the presence of additional cnidarian specific genes and characterized these genes within a phylogenetic context.ResultsIllumina assemblies of transcriptome or genome data of three myxozoan species (Enteromyxum leei, Kudoa iwatai, and Sphaeromyxa zaharoni) and of the enigmatic cnidarian parasite Polypodium hydriforme (Polypodiozoa) were mined using tBlastn searches with nematocyst-specific proteins as queries. Several orthologs of nematogalectins and minicollagens were identified. Our phylogenetic analyses indicate that myxozoans possess three distinct minicollagens. We found that the cnidarian repertoire of nematogalectins is more complex than previously thought and we identified additional members of the nematogalectin family. Cnidarians were found to possess four nematogalectin/ nematogalectin-related genes, while in myxozoans only three genes could be identified.ConclusionsOur results demonstrate that myxozoans possess a diverse array of genes that are taxonomically restricted to Cnidaria. Characterization of these genes provide compelling evidence that polar capsules and nematocysts are homologous structures and that myxozoans are highly degenerate cnidarians. The diversity of minicollagens was higher than previously thought, with the presence of three minicollagen genes in myxozoans. Our phylogenetic results suggest that the different myxozoan sequences are the results of ancient divergences within Cnidaria and not of recent specializations of the polar capsule. For both minicollagen and nematogalectin, our results show that myxozoans possess less gene copies than their cnidarian counter parts, suggesting that the polar capsule gene repertoire was simplified with their reduced body plan.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-014-0205-0) contains supplementary material, which is available to authorized users.
Our study reveals a hitherto overlooked ecological threat of climate change. Studies of warming events in the ocean have typically focused on the events’ maximum temperature and duration as the cause of devastating disturbances in coral reefs, kelp forests, and rocky shores. In this study, however, we found that the rate of onset (Ronset), rather than the peak, was the likely trigger of mass mortality of coral reef fishes in the Red Sea. Following a steep rise in water temperature (4.2 °C in 2.5 d), thermally stressed fish belonging to dozens of species became fatally infected by Streptococcus iniae. Piscivores and benthivores were disproportionately impacted whereas zooplanktivores were spared. Mortality rates peaked 2 wk later, coinciding with a second warming event with extreme Ronset. The epizootic lasted ∼2 mo, extending beyond the warming events through the consumption of pathogen-laden carcasses by uninfected fish. The warming was widespread, with an evident decline in wind speed, barometric pressure, and latent heat flux. A reassessment of past reports suggests that steep Ronset was also the probable trigger of mass mortalities of wild fish elsewhere. If the ongoing increase in the frequency and intensity of marine heat waves is associated with a corresponding increase in the frequency of extreme Ronset, calamities inflicted on coral reefs by the warming oceans may extend far beyond coral bleaching.
Streptococcus iniae was isolated from 2 moribund wild Red Sea fishes, Pomadasys stridens (Pomadasyidae) and Synodus variegatus (Synodontidae), both collected in shallow waters along the Israeli coast of the Gulf of Eilat. The site is approximately 2 km from a mariculture cage farm in which streptococcal infections were diagnosed in previous years in the red drum Sciaenops ocellatus. This is the first report of S. iniae in Red Sea fishes. Biochemical and molecular similarities between the isolates from cultured fishes and those from the wild specimens suggest that a single strain is involved, and that 'amplification' and dispersal of this pathogen from captive to feral fishes have occurred. At the molecular level, the pathogen is different from the S. iniae isolates that have been afflicting the Israeli freshwater aquaculture in recent years. Although S. iniae prevalence in the wild fish populations of the area remains to be determined, the northernmost region of the Gulf of Eilat, virtually landlocked and with generally calm seas and weak currents, seems to be particularly vulnerable to the impact of diseases that develop in this mariculture system. KEY WORDS: Fish disease · Mariculture · Red drum · Sciaenops ocellatus · Sea bass · Dicentrarchus labrax · Tilapia · Oreochromis mossambicus · 16S rRNA · PCR Resale or republication not permitted without written consent of the publisherDis Aquat Org 49: [165][166][167][168][169][170] 2002 populations increases the opportunity for disease transmission in both directions, since translocated species may not only be extremely sensitive to a local pathogen but may themselves carry exotic diseases that can spread to indigenous wild populations (Paperna 1998).In the Eilat region, streptococcosis has recurred repeatedly since it was first diagnosed in 1996 in the red drum (see Table 1). During the summer of 2000, persistent mortalities of wild fishes in the shallow waters of Eilat's northern coast were investigated. Gram-positive cocci in chains were isolated from 2 moribund wild specimens and compared with streptococcal isolates from fishes cultured in this region in previous years. MATERIALS AND METHODS Fishes.The infection chronology, sources of isolation and list of fish hosts are summarized in Table 1. The first case was diagnosed in 1995 in a stock of European sea bass Dicentrarchus labrax submitted to our laboratory for examination from a fish farm in Ashdod, on the Mediterranean coast of Israel. All subsequent cases refer to fish grown in the Eilat area (Red Sea). Water in this region is subjected to limited seasonal fluctuations of temperature (23 ± 1.5°C) and salinity (40 ± 1 ‰). Red drum Sciaenops ocellatus were examined during mortality outbreaks in the cages. The tilapia Oreochromis mossambicus, adapted to seawater, were maintained at Israel Oceanographic and Limnological Research National Center for Mariculture in the facilities of the Reproduction Department for experimental purposes. The lined piggy Pomadasys stridens (Pomadasyidae) and the lizar...
Myxozoans are a large group of poorly characterized cnidarian parasites. To gain further insight into their evolution, we sequenced the mitochondrial (mt) genome of Enteromyxum leei and reevaluate the mt genome structure of Kudoa iwatai. Although the typical animal mt genome is a compact, 13-25 kb, circular chromosome, the mt genome of E. leei was found to be fragmented into eight circular chromosomes of ∼23 kb, making it the largest described animal mt genome. Each chromosome was found to harbor a large noncoding region (∼15 kb), nearly identical between chromosomes. The protein coding genes show an unusually high rate of sequence evolution and possess little similarity to their cnidarian homologs. Only five protein coding genes could be identified and no tRNA genes. Surprisingly, the mt genome of K. iwatai was also found to be composed of two chromosomes. These observations confirm the remarkable plasticity of myxozoan mt genomes.
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