Predicted Redistribution of Ceratomyxa shasta Genotypes with Salmonid Passage in the Deschutes River, Oregon

Aseries of dams on the Deschutes River, Oregon, act as migration barriers that segregate the river system into upper and lower basins. Proposed fish passage between basins would reunite populations of native potamodromous fish and allow anadromous fish of Deschutes River origin access to the upper basin. We assessed the potential redistribution of host-species-specific genotypes (O, I, II, III) of the myxozoan parasite Ceratomyxa shasta that could occur with fish passage and examined the influence of nonnative fish on genotype composition. To determine the present distribution of the parasite genotypes, we exposed eight salmonid species—three native and five stocked for sport fishing—in present and predicted anadromous salmonid habitats. We monitored fish for infection by C. shasta and sequenced a section of the parasite ribosomal DNA gene from fish and water samples to determine parasite genotype. Genotype O was present in both upper and lower basins and detected only in steelhead Oncorhynchus mykiss. Genotype I was spatially limited to the lower basin, isolated predominately from Chinook salmon O. tshawytscha, and lethal for this species only. Genotype II was detected in both basins and in multiple species, but only as a minor component of the infection. Genotype III was also present in both basins, had a wide host range, and caused mortality in native steelhead and multiple nonnative species. Atlantic salmon Salmo salar and kokanee O. nerka were the least susceptible to infection by any genotype of C. shasta. Our findings confirmed the host-specific patterns of C. shasta infections and indicated that passage of Chinook salmon would probably spread genotype I into the upper Deschutes River basin, but with little risk to native salmonid populations.Keywords: Chinook, Basin, Myxozoa, Rainbow trout, Mortality, Assay, Infection, Myxosporean parasite, Host, Oncorhynchus tshawytsch

Relationship Between Temperature and Ceratomyxa shasta–Induced Mortality In Klamath River Salmonids

Water temperature influences almost every biological and physiological process of salmon, including disease resistance. In the Klamath River (California), current thermal conditions are considered sub-optimal for juvenile salmon. In addition to borderline temperatures, these fish must contend with the myxozoan parasite Ceratomyxa shasta, a significant cause of juvenile salmonid mortality in this system. This paper presents 2 studies, conducted from 2007 to 2010, that examine thermal effects on C. shasta induced mortality in native Klamath River Chinook (Oncorhynchus tshawytscha) and coho (Oncorhynchus kisutch) salmon. In each study, fish were exposed to C. shasta in the Klamath River for 72 hr and then reared in the laboratory under temperature-controlled conditions. The first study analyzed data collected from a multi-year monitoring project to asses the influence of elevated temperatures on parasite-induced mortality during the spring/summer migration period. The second study compared disease progression in both species at 4 temperatures (13, 15, 18, and 21 C) representative of spring/summer migration conditions. Both studies demonstrated that elevated water temperatures consistently resulted in higher mortality and faster mean days to death. However, analysis of data from the multi-year monitoring showed that the magnitude of this effect varied among years and was more closely associated with parasite density than with temperature. Also, there was a difference in the timing of peak mortality between species; Chinook incurred high mortalities in 2008 and 2009, whereas coho was greatest in 2007 and 2008. As neither temperature nor parasite density can be easily manipulated, management strategies should focus on disrupting the overlap of this parasite and its obligate hosts to improve emigration success and survival of juvenile salmon in the Klamath River.Keywords: Rainbow trout, Water temperature, Myxozoa, Myxosporean parasite, Coho salmon, Steelhead, California, Assay, Chinook salmo

Dam Removal and Implications for Fish Health: Ceratomyxa shasta in the Williamson River, Oregon, USA

The removal of dams on a river is one potential tool for the ecological restoration of native salmonid fishes. However, the removal of barriers also introduces risks, such as the introduction of fish pathogens into previously isolated populations. The proposed removal of four dams on the Klamath River, Oregon–California, provides an opportunity for examining the disease risks associated with dam removal. A salmonid pathogen endemic to the region, Ceratomyxa shasta, is responsible for high mortality in juvenile Chinook salmon Oncorhynchus tshawytscha and coho salmon O. kisutch below the dams. Above the dams, parasite densities are lower and not implicated in salmonid mortality, except in the Williamson River tributary, where high parasite densities raise concerns over the restoration of anadromous fish that are likely to take advantage of spawning habitat in that river. In the current study, baseline information on parasite density, distribution, and genotype composition in the Williamson River was gathered to determine how salmonid reintroduction might be affected by parasite dynamics. Assay of water samples highlighted two areas of high parasite density: between the mouth of the Williamson River and the confluence of the Sprague River tributary, and above the Spring Creek confluence. Despite these high parasite densities, mortality did not occur in sentinel coho or Chinook salmon. Genetic analyses of parasites from water samples and infected fish demonstrated that C. shasta genotype II was dominant and was associated with stocked nonnative rainbow trout O. mykiss. The absence of pathogenicity of this parasite genotype for Chinook and coho salmon suggests that reintroduction plans will not initially be adversely affected by the high parasite densities in the Williamson River. However, following dam removal, returning adult salmon will transport parasite genotypes present below the dams upstream. These genotypes are likely to become established and may reach densities that could affect juvenile Chinook and coho salmon.This is the publisher’s final pdf. The published article is copyrighted by Taylor & Francis for the American Fisheries Society and can be found at: http://www.tandfonline.com/toc/ujfm20/current

The cnidarian parasite Ceratonova shasta utilizes inherited and recruited venom-like compounds during infection

Background 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. Methods 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. Results 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 diversity 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

Widespread distribution of Ceratonova shasta (Cnidaria: Myxosporea) genotypes indicates evolutionary adaptation to its salmonid fish hosts

The distribution of the freshwater myxozoan parasite Ceratonova shasta in the Pacific Northwest of North America is limited to overlap in the ranges of its 2 hosts: the polychaete Manyunkia sp., and Pacific salmonids. Studies in the Klamath River (Oregon/California) and Deschutes River (Oregon), showed that the parasite population is comprised of multiple sympatric genotypes, some of which correlate with particular salmonid host species and with differences in clinical disease in those hosts. The 3 primary genotypes O, I, and II are defined by the number of a specific tri-nucleotide repeat in the internal transcribed spacer-1 region. To understand the spatial extent of host-parasite genotype patterns, we sequenced the parasite from 448 salmonid fishes from river basins in California, Oregon, Washington, Idaho, and British Columbia, Canada. We sampled intestinal tissues from 6 species of salmon and trout, both those that exist naturally with the parasite (sympatric) and those that do not naturally co-occur with the parasite and were exposed artificially in cages (allopatric). In most river basins we detected the same primary C. shasta genotypes that were described from the Klamath and Deschutes rivers, and we did not detect any novel primary genotypes. Host- parasite genotype patterns were consistent with previous data: genotype O was found in sympatric trout only; genotype I predominantly in Chinook salmon, and genotype II in all 6 fish species but dominant in coho salmon. Our findings of widespread, consistent host-parasite genotype patterns support the hypothesis that C. shasta has a long evolutionary history with salmonid fishes in the Pacific Northwest, and impels additional studies to determine if these parasite genotypes should be considered different species

Evolutionary Analysis of Cystatins of Early-Emerging Metazoans Reveals a Novel Subtype in Parasitic Cnidarians

Acknowledgments: We thank to Baveesh Pudhuvai (BC CAS, Budweis, Czech Republic) for help in the PCR verification of Buddenbrockia stefin. We also thank Ivan Fiala (BC CAS, Budweis, Czech Republic) for providing suggestions to improve the manuscript and for sharing M. lieberkuehni and N. pickii transcriptomic data. We are grateful to Hanna Hartikainen (ETH Zurich, Switzerland) for sharing T. bryosalmonae genome data. Funding: This research was funded by the Ministry of Education, Youth, and Sports of the Czech Republic, grant number LTAUSA17201; by the European Commission under the H2020 Programme— ParaFishControl, grant number 634429; by the Czech Science Foundation, grant number 19-28399X (to A. S. Holzer, G. Alama-Bermejo, and J. Kyslík) and 21-16565S and by the Czech Academy of Sciences and Hungarian Academy of Sciences, grant number MTA 19-07. This publication reflects the views of the authors only; the European Commission cannot be held responsible for any use which may be made of the information contained therein.Peer reviewedPublisher PD