Highlights d The origin of apicomplexans from algae occurred at least three times independently d Piridium and Platyproteum form distinct lineages of obligate animal parasites d They both retain cryptic plastids that are highly convergent with apicomplexans
BackgroundCommercial 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.MethodsLumpfish from the Icelandic coast were examined for the causative agent of kidney enlargement. Fish were dissected and used in histological and molecular studies.ResultsLumpfish, with various grades of clinical signs, were observed at 12 of the 43 sites sampled around Iceland. From a total of 77 fish examined, 18 had clear clinical signs, the most prominent of which was an extensive enlargement and pallor of the kidneys. The histopathology of the most severely affected fish consisted of extensive degeneration and necrosis of kidney tubules and vacuolar degeneration of the haematopoietic tissue. Intranuclear microsporidians were detected in all organs examined in fish with prominent clinical signs and most organs of apparently healthy fish using the new PCR and histological examination. One or multiple uniformly oval shaped spores measuring 3.12 ± 0.15 × 1.30 ± 0.12 μm were observed in the nucleus of affected lymphocytes and lymphocyte precursor cells. DNA sequencing provided a ribosomal DNA sequence that was strongly supported in phylogenetic analyses in a clade containing other microsporidian parasites from the Enterocytozoonidae, showing highest similarity to the intranuclear microsporidian Nucleospora salmonis.ConclusionsIntranuclear microsporidian infections are common in wild caught lumpfish from around the Icelandic coast. Infections can cause severe clinical signs and extensive histopathological changes, but are also present, at lower levels, in fish that do not show clinical signs. Some common features exist with the intranuclear microsporidian previously reported from captive Canadian lumpfish, but DNA sequence data is required from Canadian fish to confirm conspecificity.Based on phylogenetic analysis and the intranuclear location of the parasite, the name Nucleospora cyclopteri n. sp. is proposed.
"X-cells" have long been associated with tumor-like formations (xenomas) in marine fish, including many of commercial interest. The name was first used to refer to the large polygonal cells that were found in epidermal xenomas from flatfish from the Pacific Northwest [1]. Similar looking cells from pseudobranchial xenomas had previously been reported from cod in the Atlantic [2] and Pacific Oceans [3]. X-cell pathologies have been reported from five teleost orders: Pleuronectiformes (flatfish), Perciformes (perch-like fish), Gadiformes (cods), Siluriformes (catfish), and Salmoniformes (salmonids). Various explanations have been elicited for their etiology, including being adenomas or adenocarcinomas [4, 5], virally transformed fish cells [6-8], or products of coastal pollution [9, 10]. It was hypothesized that X-cells were protozoan parasites [1, 11-13], and although recent molecular analyses have confirmed this, they have failed to place them in any phylum [14-18], demonstrating weak phylogenetic associations with the haplosporidians [16] or the alveolates [15]. Here, we sequenced rRNA genes from European and Japanese fish that are known to develop X-cell xenomas. We also generated a metagenomic sequence library from X-cell xenomas of blue whiting and Atlantic cod and assembled 63 X-cell protein-coding genes for a eukaryote-wide phylogenomic analysis. We show that X-cells group in two highly divergent clades, robustly sister to the bivalve parasite Perkinsus. We formally describe these as Gadixcellia and Xcellia and provide a phylogenetic context to catalyze future research. We also screened Atlantic cod populations for xenomas and residual pathologies and show that X-cell infections are more prevalent and widespread than previously known.
Apicomplexans are a diverse group of globally important parasites, that include pathogens like Plasmodium, the causative agent of malaria. Despite their current obligate parasitic nature, apicomplexans evolved from photosynthetic algae and retain a remnant plastid (chloroplast). Such a complex evolutionary transition was unexpected, but here we show that it occurred at least three times independently. Using single-cell genomics and transcriptomics from 25 diverse uncultivated parasites, we find that two genera previously classified within the Apicomplexa, Piridium and Platyproteum, form separately branching lineages in phylogenomic analyses. Both retain cryptic plastids with genomic and metabolic features convergent with apicomplexans. These findings suggest a predilection in this lineage for both the loss of photosynthesis and the transition to a morphologically similar parasitic lifestyle, resulting in 30 multiple lineages of highly convergent animal parasites. Main Text:The apicomplexans are a group of obligate animal pathogens that include Plasmodium (malaria), Toxoplasma (toxoplasmosis) and Cryptosporidium (cryptosporidiosis)(1). They are united by a complex and distinctive suite of cytoskeletal and secretory structures related to 35 infection called the apical complex, which are used to recognize and gain entry into animal host cells. Apicomplexans are known to have evolved from free-living photosynthetic ancestors and retain a relict plastid (the apicoplast), which is non-photosynthetic, but houses a number of other essential metabolic pathways(2). The closest relatives of apicomplexans includes a mix of both photosynthetic algae (chromerids) as well as non-photosynthetic microbial predators 40 (colpodellids)(3), and genomic analyses of these free-living relatives have revealed a great deal about how such a dramatic transition may have taken place, as well as how parasitism originates more generally(4). 45
BackgroundApproximately 40 species of Sphaeromyxa have been described, all of which are coelozoic parasites from gall bladders of marine fish. They are unique amongst the myxosporeans as they have polar filaments that are flat and folded instead of being tubular and spirally wound. This unusual feature was used as a subordinal character to erect the suborder Sphaeromyxina, which contains one family, the Sphaeromyxidae, and a single genus Sphaeromyxa.MethodsIn the present study, we examine eelpout from the genus Lycodes from Iceland for the presence of myxosporean parasites in the gall bladder and perform morphological and DNA studies.ResultsA novel myxosporean, Sphaeromyxa lycodi n. sp., was identified in the gall bladders of five of the six species of Lycodes examined, with a prevalence ranging from 29 - 100%. The coelozoic plasmodia are large, polysporous and contain disporic pansporoblasts and mature spores which are arcuate. The pyriform polar capsules encase long and irregularly folded ribbon-like polar filaments. Each spore valve has two distinct ends and an almost 180° twist along the relatively indistinct suture line. The single sporoplasm is granular with two nuclei. Sphaeromyxa lycodi is phylogenetically related to other arcuate sphaeromyxids and is reproducibly placed with all known sphaeromyxids and forms part of a robustly supported clade of numerous myxosporean genera which infect the hepatic biliary systems of a wide range of hosts.ConclusionsSphaeromyxa lycodi is a common gall bladder myxosporean in eelpout of the genus Lycodes from Northern Iceland. It has characteristics typical of the genus and develops arcuate spores. Molecular phylogenetic analyses confirm that sphaeromyxids form a monophyletic group, subdivided into straight and arcuate spore forms, within the hepatic biliary clade that infect a wide range of freshwater associated animals. The ancestral spore form for the hepatic biliary clade was probably a Chloromyxum morphotype; however, sphaeromyxids have more recently evolved from an ancestor with a spindle-shaped Myxidium spore form. We recommend that the suborder Sphaeromyxina is suppressed; however, we retain the family Sphaeromyxidae and place it in the suborder Variisporina.
The phylum Apicomplexa consists largely of obligate animal parasites that include the causative agents of human diseases such as malaria. Apicomplexans have also emerged as models to study the evolution of non-photosynthetic plastids, as they contain a relict chloroplast known as the apicoplast. The apicoplast offers important clues into how apicomplexan parasites evolved from free-living ancestors and can provide insights into reductive organelle evolution. Here, we sequenced the transcriptomes and apicoplast genomes of three deep-branching apicomplexans, Margolisiella islandica, Aggregata octopiana and Merocystis kathae. Phylogenomic analyses show that these taxa, together with Rhytidocystis, form a new lineage of apicomplexans that is sister to the Coccidia and Hematozoa (the lineages including most medically significant taxa). Members of this clade retain plastid genomes and the canonical apicomplexan plastid metabolism. However, the apicoplast genomes of Margolisiella and Rhytidocystis are the most reduced of any apicoplast, are extremely GC-poor, and have even lost genes for the canonical plastidial RNA polymerase. This new lineage of apicomplexans, for which we propose the class Marosporida class nov., occupies a key intermediate position in the apicomplexan phylogeny, and adds a new complexity to the models of stepwise reductive evolution of genome structure and organelle function in these parasites.
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