ORCID Profile
0000-0002-7180-6672
Current Organisation
Oregon State University
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Publisher: MDPI AG
Date: 03-02-2021
Abstract: The evolutionary aspects of cystatins are greatly underexplored in early-emerging metazoans. Thus, we surveyed the gene organization, protein architecture, and phylogeny of cystatin homologues mined from 110 genomes and the transcriptomes of 58 basal metazoan species, encompassing free-living and parasite taxa of Porifera, Placozoa, Cnidaria (including Myxozoa), and Ctenophora. We found that the cystatin gene repertoire significantly differs among phyla, with stefins present in most of the investigated lineages but with type 2 cystatins missing in several basal metazoan groups. Similar to liver and intestinal flukes, myxozoan parasites possess atypical stefins with chimeric structure that combine motifs of classical stefins and type 2 cystatins. Other early metazoan taxa regardless of lifestyle have only the classical representation of cystatins and lack multi-domain ones. Our comprehensive phylogenetic analyses revealed that stefins and type 2 cystatins clustered into taxonomically defined clades with multiple independent paralogous groups, which probably arose due to gene duplications. The stefin clade split between the subclades of classical stefins and the atypical stefins of myxozoans and flukes. Atypical stefins represent key evolutionary innovations of the two parasite groups for which their origin might have been linked with ancestral gene chimerization, obligate parasitism, life cycle complexity, genome reduction, and host immunity.
Publisher: PeerJ
Date: 17-08-2018
DOI: 10.7287/PEERJ.PREPRINTS.26819V2
Abstract: Research Infrastructures (RIs) are facilities, resources and services used by the scientific community to conduct research and foster innovation. LifeWatch ERIC has developed various virtual research environments, which include many virtual laboratories (vLabs) offering high computational capacity and comprehensive collaborative platforms that supporting the needs of digital bio ersity science. Over its 250 years of history, the taxonomic research community has developed a system for describing, classifying and naming taxa across multiple levels. For the marine biota, taxonomic information is organized and made publicly available through the World Register of Marine Species (WoRMS) that records more than 250,000 described valid species. Although scientists tend to assign an equal status (in terms of contribution to overall ersity) to each taxon used in taxonomy, biogeography, ecology and bio ersity, the question “ are all taxa equal? ” has never been tested at a global scale. We present evidence that this question can be addressed by applying relatedness indices (Taxonomic Distinctness) over the entire WoRMS metazoan tree. The RvLab, developed by the LifeWatchGreece RI, operating on a high-performance computer cluster, has been used to meet the high computational demands required for such an analysis at a global scale.
Publisher: PeerJ
Date: 15-12-2021
DOI: 10.7717/PEERJ.12606
Abstract: Cnidarians are the most ancient venomous organisms. They store a cocktail of venom proteins inside unique stinging organelles called nematocysts. When a cnidarian encounters chemical and physical cues from a potential threat or prey animal, the nematocyst is triggered and fires a harpoon-like tubule to penetrate and inject venom into the prey. Nematocysts are present in all Cnidaria, including the morphologically simple Myxozoa, which are a speciose group of microscopic, spore-forming, obligate parasites of fish and invertebrates. Rather than predation or defense, myxozoans use nematocysts for adhesion to hosts, but the involvement of venom in this process is poorly understood. Recent work shows some myxozoans have a reduced repertoire of venom-like compounds (VLCs) relative to free-living cnidarians, however the function of these proteins is not known. We searched for VLCs in the nematocyst proteome and a time-series infection transcriptome of Ceratonova shasta , a myxozoan parasite of salmonid fish. We used four parallel approaches to detect VLCs: BLAST and HMMER searches to preexisting cnidarian venom datasets, the machine learning tool ToxClassifier, and structural modeling of nematocyst proteomes. Sequences that scored positive by at least three methods were considered VLCs. We then mapped their time-series expressions in the fish host and analyzed their phylogenetic relatedness to sequences from other venomous animals. We identified eight VLCs, all of which have closely related sequences in other myxozoan datasets, suggesting a conserved venom profile across Myxozoa, and an overall reduction in venom ersity relative to free-living cnidarians. Expression of the VLCs over the 3-week fish infection varied considerably: three sequences were most expressed at one day post-exposure in the fish’s gills whereas expression of the other five VLCs peaked at 21 days post-exposure in the intestines, coinciding with the formation of mature parasite spores with nematocysts. Expression of VLC genes early in infection, prior to the development of nematocysts, suggests venoms in C. shasta have been repurposed to facilitate parasite invasion and proliferation within the host. Molecular phylogenetics suggested some VLCs were inherited from a cnidarian ancestor, whereas others were more closely related to sequences from venomous non-Cnidarian organisms and thus may have gained qualities of venom components via convergent evolution. The presence of VLCs and their differential expression during parasite infection enrich the concept of what functions a “venom” can have and represent targets for designing therapeutics against myxozoan infections.
Publisher: Proceedings of the National Academy of Sciences
Date: 24-02-2020
Abstract: Although aerobic respiration is a hallmark of eukaryotes, a few unicellular lineages, growing in hypoxic environments, have secondarily lost this ability. In the absence of oxygen, the mitochondria of these organisms have lost all or parts of their genomes and evolved into mitochondria-related organelles (MROs). There has been debate regarding the presence of MROs in animals. Using deep sequencing approaches, we discovered that a member of the Cnidaria, the myxozoan Henneguya salminicola, has no mitochondrial genome, and thus has lost the ability to perform aerobic cellular respiration. This indicates that these core eukaryotic features are not ubiquitous among animals. Our analyses suggest that H. salminicola lost not only its mitochondrial genome but also nearly all nuclear genes involved in transcription and replication of the mitochondrial genome. In contrast, we identified many genes that encode proteins involved in other mitochondrial pathways and determined that genes involved in aerobic respiration or mitochondrial DNA replication were either absent or present only as pseudogenes. As a control, we used the same sequencing and annotation methods to show that a closely related myxozoan, Myxobolus squamalis , has a mitochondrial genome. The molecular results are supported by fluorescence micrographs, which show the presence of mitochondrial DNA in M. squamalis , but not in H. salminicola. Our discovery confirms that adaptation to an anaerobic environment is not unique to single-celled eukaryotes, but has also evolved in a multicellular, parasitic animal. Hence, H. salminicola provides an opportunity for understanding the evolutionary transition from an aerobic to an exclusive anaerobic metabolism.
Publisher: Cambridge University Press (CUP)
Date: 14-07-2020
DOI: 10.1017/S0031182020001158
Abstract: Myxozoans are parasitic, microscopic cnidarians that have retained the phylum-characteristic stinging capsules called nematocysts. Free-living cnidarians, like jellyfish and corals, utilize nematocysts for feeding and defence, with discharge powered by osmotic energy. Myxozoans use nematocysts to anchor to their fish hosts in the first step of infection, however, the discharge mechanism is poorly understood. We used Myxobolus cerebralis , a pathogenic myxozoan parasite of salmonid fishes, and developed two assays to explore the nature of its nematocyst discharge. Using parasite actinospores, the infectious stage to fish, we stimulated discharge of the nematocysts with rainbow trout mucus in vitro , in solutions enriched with chloride salts of Na + , K + , Ca 2+ and Gd 3+ , and quantified discharge using microscopy. We then used quantitative polymerase chain reaction to evaluate the in vivo effects of these treatments, plus Mg 2+ and the common aquaculture disinfectant KMnO₄, on the ability of M. cerebralis actinospores to infect fish. We found that Mg 2+ and Gd 3+ reduced infection in vivo , whereas Na + and K + over-stimulated nematocyst discharge in vitro and reduced infection in vivo . These findings align with nematocyst discharge behaviour in free-living Cnidaria, and suggest phylum-wide commonalties, which could be exploited to develop novel approaches for controlling myxozoan diseases in aquaculture.
Publisher: MDPI AG
Date: 24-05-2023
DOI: 10.3390/D15060702
Abstract: We used a combination of morphological, molecular and biological data to characterize a novel Henneguya (Myxozoa) species infecting the Amazonian prochilodontid Semaprochilodus insignis or “kissing prochilodus”, a popular food fish and aquarium species in the Brazilian Amazon. Twenty-one S. insignis were caught live from the Tapajós river, Pará State, Brazil, then examined for myxozoan infections. Cysts of a novel Henneguya species were observed in the connective tissue of the fins. Myxospores measured 48 ± 4.9 (39.5–60.8) µm total length, of which caudal appendages were 33 ± 4.5 (26.4–45.2) µm and spore body was 15 ± 1.6 (12.4–20.5) µm. The spore body was 4.0 ± 0.6 (2.7–5.3) µm wide × 3.2 ± 0.4 (2.7–3.6) µm thick, with two unequal polar capsules (nematocysts) 7.2 ±0.8 (5.2–8.3) × 1.5 ± 0.3 (1.0–2.2) µm for the larger capsule and 5 ± 0.7 (4.0–6.3) × 1.4 ± 0.2 (1.0–1.8) µm for the smaller capsule. Polar tubules had 8–13 turns. Generative cells, immature and mature myxospores were observed within plasmodia. Ultrastructure showed plasmodia surrounded by collagen fibers, with the plasmodial membrane having pinocytotic channels. Phylogenetic analysis of small subunit ribosomal DNA sequences showed that the new Henneguya species clustered as a sister taxon to Henneguya tietensis, a parasite of the gills of the prochilodontid fish Prochilodus lineatus, from the geographically distant Paraná–Paraguai River basin.
Publisher: Informa UK Limited
Date: 21-11-2018
Publisher: Informa UK Limited
Date: 02-07-2020
Publisher: Oxford University Press (OUP)
Date: 08-09-2020
Abstract: DNA cytosine methylation is central to many biological processes, including regulation of gene expression, cellular differentiation, and development. This DNA modification is conserved across animals, having been found in representatives of sponges, ctenophores, cnidarians, and bilaterians, and with very few known instances of secondary loss in animals. Myxozoans are a group of microscopic, obligate endoparasitic cnidarians that have lost many genes over the course of their evolution from free-living ancestors. Here, we investigated the evolution of the key enzymes involved in DNA cytosine methylation in 29 cnidarians and found that these enzymes were lost in an ancestor of Myxosporea (the most speciose class of Myxozoa). Additionally, using whole-genome bisulfite sequencing, we confirmed that the genomes of two distant species of myxosporeans, Ceratonova shasta and Henneguya salminicola, completely lack DNA cytosine methylation. Our results add a notable and novel taxonomic group, the Myxosporea, to the very short list of animal taxa lacking DNA cytosine methylation, further illuminating the complex evolutionary history of this epigenetic regulatory mechanism.
Publisher: Wiley
Date: 29-04-2021
DOI: 10.1002/AAH.10125
Abstract: Recent range expansions of whirling disease impelled us to understand the impacts of its causative agent, the myxozoan parasite Myxobolus cerebralis , on lesser‐studied fish hosts. Mountain Whitefish Prosopium williamsoni overlap broadly with M. cerebralis across the western United States and Canada, and populations have experienced widespread declines since the 1990s. To evaluate effects of the parasite on Mountain Whitefish, we revisit formerly unpublished work of the Colorado Division of Wildlife (now Colorado Parks and Wildlife), comparing infection in age‐matched Mountain Whitefish, Rainbow Trout Oncorhynchus mykiss , and Brown Trout Salmo trutta . To complement the original report, we reanalyze mortality data and include additional SEM imagery. Infection of M. cerebralis in juvenile Mountain Whitefish was characterized by a brief but heavy period of mortality in the first 2 weeks after exposure, with limited pathology. This clinical effect is unique among the known salmonid hosts of M. cerebralis .
Publisher: Springer Science and Business Media LLC
Date: 14-01-2020
DOI: 10.1007/S00436-019-06585-3
Abstract: We surveyed introduced yellow perch Perca flavescens (Mitchill, 1814) from the Willamette River, OR, USA, to determine if these fish have co-introduced myxosporean parasites. Mature parasite myxospores were observed in brains of 3/19 fish, and were morphologically and molecularly consistent with Myxobolus neurophilus (Guilford 1963), a parasite known from yellow perch in their native range. We identified another Myxobolus species from the gill filaments of 1/22 fish. The spores from the gill filaments were oval-shaped, 11.7 (10.7-12.3) μm long × 8.6 (7.7-9.0) μm wide × 5.2 (4.6-5.6) μm thick, with two oval-shaped polar capsules 5.7 (5.1-6.5) μm × 2.7 (2.4-3.2) μm, each containing a polar tubule with 8-9 turns. Small-subunit ribosomal DNA sequences from each of four plasmodia were identical, and 4.0% different (over 1800 nucleotides) from the closest known myxosporeans. Interestingly, these sequences had overlapping peaks in their chromatograms, which suggested that DNA from multiple species was present. Hence, we isolated and sequenced three in idual myxospores and found that they too had mixed chromatograms, which indicated presence of at least two sequence types of small-subunit ribosomal DNA in each spore (GenBank accession MK592012, MK592013), a rare character among described myxosporeans. The spore morphology, morphometry, tissue tropism, and DNA sequence supported a diagnosis of a novel species, Myxobolus doubleae n. sp. This parasite is unknown from yellow perch in its native range, despite extensive historical surveys, which suggests that introduced yellow perch might have acquired an endemic Myxobolus species via spillback from another fish host.
Publisher: Elsevier BV
Date: 08-2018
DOI: 10.1016/J.ZOOL.2018.06.005
Abstract: Myxozoans are endoparasites with complex life cycles that alternate between invertebrate and vertebrate hosts. Though considered protozoans for over 150 years, they are now recognized as metazoans, given their multicellularity and ultrastructural features. In recognition of synapomorphies and cnidarian-specific genes, myxozoans were placed recently within the phylum Cnidaria. Although they have lost genetic and structural complexity on the path to parasitism, myxozoans have retained characteristic cnidarian cnidocysts, but use them for initiating host infection. Myxozoans represent at least 20% of phylum Cnidaria, but as a result of rapid evolution, extensive ersification and host specialization, they are probably at least as erse as their free-living relatives. The ability of myxozoans to infect freshwater, marine and terrestrial hosts implies that Cnidaria are no longer constrained to the aquatic environment.
No related grants have been discovered for Stephen Atkinson.