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A new species of Myxobolus (Myxozoa: Bivalvulida) infecting the medulla oblongata and nerve cord of brook trout Salvelinus fontinalis in southern Appalachia (New River, NC, USA)

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Abstract

Myxobolus neurofontinalis n. sp. infects the brain and medulla oblongata of brook trout (Salvelinus fontinalis [Mitchill, 1814]) in the New River, western NC. It is the first species of Myxobolus described from the brook trout and resembles another congener (Myxobolus arcticus Pugachev and Khokhlov, 1979) that infects nerve tissue of chars (Salvelinus spp.). The new species differs from M. arcticus and all congeners by myxospore dimensions and by having a mucous envelope and distinctive sutural markings. A phylogenetic analysis of the small subunit rDNA (18S) suggests that the new species shares a recent common ancestor with some isolates identified as M. arcticus and that the new species and its close relatives (except Myxobolus insidiosus Wyatt and Pratt, 1973) comprise a clade of salmonid nerve-infecting myxobolids. The phylogenetic analysis indicates that several isolates of “M. arcticus” (sensu lato) in GenBank are misidentified and distantly related to other isolates taken from the type host (Oncorhynchus nerka [Walbaum, 1792]) and from nearby the type locality (Kamchatka Peninsula, Russia). Serial histological sections of infected brook trout confirmed that myxospores of the new species are intercellular and infect nerve cord and medulla oblongata only. A single infected brook trout showed an inflammatory response characterized by focal lymphocytic infiltrates and eosinophilic granulocytes; however, the remaining 4 brook trout lacked evidence of a histopathological change or demonstrable host response. These results do not support the notion that this infection is pathogenic among brook trout.

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References

  • Abdel-Ghaffar F, El-Toukhy A, Al-Quraishy S, Al-Rasheid K, Abdel-Baki AS, Hegazy A, Bashtar AR (2008) Five new myxosporean species (Myxozoa: Myxosporea) infecting Nile tilapia Oreochromis niloticus in Bahr Shebin, Nile Tributary, Nile Delta, Egypt. Parasitol Res 103:1197–1205

    CAS  PubMed  Google Scholar 

  • Andree KB, Gresoviac SJ, Hedrick RP (1997) Small subunit ribosomal RNA sequences unite alternate actinosporean and myxosporean stages of Myxobolus cerebralis the causative agent of whirling disease in salmonid fish. J Eukaryot Microbiol 44:208–215

    CAS  PubMed  Google Scholar 

  • Andree KB, MacConnell E, Hedrick RP (1998) A nested polymerase chain reaction for the detection of genomic DNA of Myxobolus cerebralis in rainbow trout Oncorhynchus mykiss. Dis Aquat Org 34:145–154

    CAS  Google Scholar 

  • Andree KB, Székely C, Molnár K, Gresoviac SJ, Hedderick RP (1999) Relationships among members of the genus Myxobolus (Myxozoa: Bivalvidae) based on small subunit ribosomal DNA sequences. J Parasitol 85:68–74

    CAS  PubMed  Google Scholar 

  • Arthur JR, Margolis L, Arai HP (1976) Parasites of fishes of Aishihik and Stevens Lakes, Yukon Territory, and potential consequences of their interlake transfer through a proposed water diversion for hydroelectrical purposes. J Fish Res Board Can 33:2489–2499

    Google Scholar 

  • Bahri S, Andree KB, Hedrick RP (2003) Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. J Eukaryot Microbiol 50:463–470

    PubMed  Google Scholar 

  • Baldwin TJ, Peterson JE, McGhee GC, Staigmiller KD, Motteram ES, Downs CC, Stanek DR (1998) Distribution of Myxobolus cerebralis in salmonid fishes in Montana. J Aquat Anim Heal 10:361–371

    Google Scholar 

  • Bartholomew JL, Reno PW (2002) The history and dissemination of whirling disease. Am Fish Soc Symp 26:1–22

    Google Scholar 

  • Barton M, Bond CE (2007) Bond’s biology of fishes, 3rd edn. Thomson Brooks, Belmont, California

    Google Scholar 

  • Bean TH (1888) Distribution and some characters of the Salmonidae. Am Nat 22:306–314

    Google Scholar 

  • Carriero MM, Adriano EA, Silva MRM, Ceccarelli PS, Maia AAM (2013) Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS ONE 8:e73713. https://doi.org/10.1371/journal.pone.0073713

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics, and parallel computing. Nat Methods 9:772

    CAS  PubMed  PubMed Central  Google Scholar 

  • Desdevises Y, Arthur JR, Pellerin-Massicotte J (1998) Parasites of anadromous arctic char (Salvelinus alpinus) from two sites in Ungava Bay (Quebec, Canada). J Helminthol Soc Wash 65:87–90

    Google Scholar 

  • Easy RH, Johnson SC, Cone DK (2005) Morphological and molecular comparison of Myxobolus procerus (Kudo,1934) and M. intramusculi n. sp. (Myxozoa) parasitizing the muscles of the trout–perch Percopsis omiscomaycus. Syst Parasitol 61:115–122

    CAS  PubMed  Google Scholar 

  • Eiras JC, Molnár K, Lu YS (2005) Synopsis of species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea: Myxobolidae). Syst Parasitol 61:1–46

    CAS  PubMed  Google Scholar 

  • Fantham HB, Porter A, Richardson LR (1939) Some Myxosporidia found in certain freshwater fishes in Quebec province, Canada. Parasitol 31:1–77

    Google Scholar 

  • Ferguson HW (2006) Systemic pathology of fish: a text and atlas of normal tissues in teleosts and their responses to disease, 2nd edn. Scotian Press, London

    Google Scholar 

  • Ferguson JA, Atkinson SD, Whipps CM, Kent ML (2008) Molecular and morphological analysis of myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. J Parasitol 94:1322–1334

    PubMed  Google Scholar 

  • Flebbe PA (1994) A regional view of the margin: salmonid abundance and distribution in the southern Appalachian Mountains of North Carolina and Virginia. Trans Am Fish Soc 123:657–667

    Google Scholar 

  • Gonzalez-Lanza C, Alvarez-Pellitero MP (1984) Myxobolus farionis n. sp. and M. ibericus of Salmo trutta from the Duero basin (NW Spain). Description and population dynamics. Angew Parasitol 25:181–189

    Google Scholar 

  • Hedrick RP, McDowell TS, Mukkatira K, Georgiadis MP, MacConnell E (1999) Susceptibility of selected inland salmonids to experimentally induced infections with Myxobolus cerebralis, the causative agent of whirling disease. J Aquat Anim Health 11:330–339

    Google Scholar 

  • Hoffman GL (1990) Myxobolus cerebralis, a worldwide cause of salmonid whirling disease. J Aquat Anim Health 2:30–37

    Google Scholar 

  • Hogge CI, Campbell MR, Johnson KA (2008a) Redescription and molecular characterization of Myxobolus kisutchi Yasutake & Wood, 1957. J Fish Dis 31:707–712

    CAS  PubMed  Google Scholar 

  • Hogge CI, Campbell MR, Johnson KA (2008b) A new species of Myxozoan (Myxosporea) from the brain and spinal cord of rainbow trout (Oncorhynchus mykiss) from Idaho. J Parasitol 94:218–222

    CAS  PubMed  Google Scholar 

  • Kaeser AJ, Rasmussen C, Sharpe WE (2006) An examination of environmental factors associated with Myxobolus cerebralis infection of wild trout in Pennsylvania. J Aquat Anim Health 18:90–100

    Google Scholar 

  • Katoh K, Standley DM (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30:772–780

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kent ML, Whitaker DJ, Margolis L (1993) Transmission of Myxobolus arcticus Pugachev and Khokhlov, 1979, a myxosporean parasite of Pacific salmon, via a triactinomyxon from the aquatic oligochaete Stylodrilus heringianus (Lumbriculidae). Can J Zoology 71:1207–1211

    Google Scholar 

  • Lom J (1969) On a new taxonomic character in Myxosporidia, as demonstrated in descriptions of two new species of Myxobolus. Folia Parasitol 16:97–103

    Google Scholar 

  • Lom J, Arthur JR (1989) A guideline for the preparation of species descriptions in Myxosporea. J Fish Dis 12:151–156

    Google Scholar 

  • Lom J, Hoffman GL (1971) Morphology of the spores of Myxosoma cerebralis (Hofer 1903) and M. cartilaginis (Hoffman, Put, and Dunbar, 1965). J Parasitol 57:1302–1308

    CAS  PubMed  Google Scholar 

  • Lorz HV, Amandi A, Banner CR, Rohovec JS (1989) Detection of Myxobolus (Myxosoma) cerebralis in salmonid fishes in Oregon. J Aquat Anim Health 1:217–221

    Google Scholar 

  • Maloney R, Crawford RJ, Markiw M, Groman D (1991) The occurrence of Myxobolus neurobius (Myxosporea) in wild young Atlantic salmon and arctic char in Newfoundland. J Aquatic Anim Health 3:146–147

    Google Scholar 

  • Markiw ME, Wolf K (1974) Myxosoma cerebralis: isolation and concentration from fish skeletal elements – sequential enzymatic digestions and purification by differential centrifugation. J Fish Res Board Can 31:15–20

    Google Scholar 

  • Nagasawa K, Urawa S, Dubinin VA (1994) A parasitological survey of sockeye salmon (Oncorhynchus nerka) and dolly varden (Salvelinus malma) from the Ozernaya River System, Kamchatka. Sci Rep Hokkaido Salmon Hatch 48:17–21

    Google Scholar 

  • Naldoni J, Zatti SA, Silva MRM, Maia AAM, Adriano EA (2019) Morphological, ultrastructural, and phylogenetic analysis of two novel Myxobolus species (Cnidaria: Myxosporea) parasitizing bryconid fish from São Francisco River, Brazil. Parasitol Int 71:27–36

    PubMed  Google Scholar 

  • Nehring RB, Walker PG (1996) Whirling disease in the wild: the new reality in the intermountain west. Fish 21:28–30

    Google Scholar 

  • Nieuwenhuys R, Pouwels E (1983) The brain stem of Actinopterygian fishes. In: Northcutt RG, Davis RE (eds) Fish Neurobiology. The University of Michigan Press, Ann Arbor, pp 25–88

    Google Scholar 

  • O’Grodnick JJ (1979) Susceptibility of various salmonids to whirling disease (Myxosoma cerebralis). Trans Am Fish Soc 108:187–190

    Google Scholar 

  • Polley TM, Atkinson SA, Jones GR, Bartholomew JL (2013) Supplemental description of Myxobolus squamalis (Myxozoa). J Parasitol 99:725–728

    PubMed  Google Scholar 

  • Power G (2002) Charrs, glaciation and seasonal ice. Environ Biol Fish 64:17–35

    Google Scholar 

  • Pugachev ON, Khokhlov PP (1979) Myxosporea of the genus Myxobolus–parasites of the salmonids head and spinal brain. In Systematic and ecology of fish from continental water bodies of the Far East Region. Vladivostok, pp 137–139 (In Russian)

  • Rambaut A, Suchard MA, Xie D, Drummond AJ (2014) FigTree:v1.4.3 Available from http://tree.bio.ed.ac.uk/software/figtree

  • Rambaut A, Drummond AJ, Xie D, Baele G, Suchard MA (2018) Posterior summarization in bayesian phylogenetics using Tracer 1.7. Syst Biol 67:901–904

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinform 19:1572–1574

    CAS  Google Scholar 

  • Ruiz CF, Rash JM, Arias CR, Besler DA, Orélis-Ribeiro R, Womble MR, Roberts JR, Warren MB, Ray CL, Lafrentz S, Bullard SA (2017) Morphological and molecular confirmation of Myxobolus cerebralis myxospores infecting wild–caught and cultured trout in North Carolina (SE USA). Dis Aquat Org 126:185–198

    CAS  Google Scholar 

  • Thompson KG, Nehring RB, Bowden DC, Wygant T (1999) Field exposure of seven species or subspecies of salmonids to Myxobolus cerebralis in the Colorado River, Middle Park, Colorado. J Aquat Anim Health 11:312–329

    Google Scholar 

  • Urawa S, Iida Y, Freeman MA, Yanagida T, Karlsbakk E, Yokoyama H (2009) Morphology and molecular comparisons of Myxobolus spp. in the nerve tissues of salmonids with the description of Myxobolus murakamii n. sp., the causative agent of myxosporean sleeping disease. Fish Pathol 44:72–80

    Google Scholar 

  • US Fish and Wildlife Service and American Fisheries Society – Fish Health Section (2014) Myxobolus cerebralis (whirling disease). In: AFS-FHS Blue Book Section 2: USFWS/AFS-FHS standard procedure for aquatic animal health inspections. American Fisheries Society – Fish Health Section, Bethesda, MD, p. 1–13

  • Vincent ER (1996) Whirling disease and wild trout: the Montana experience. Fish 21:32–33

    Google Scholar 

  • Yokoyama H, Kageyama T, Ohara K, Yanagida T (2007) Myxobolus nagaraensis n. sp. (Myxozoa: Myxozporea) causes abdominal distension of freshwater goby Phinogobius sp. OR type from the Nagara River. Fish Sci 73:633–639

    CAS  Google Scholar 

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Acknowledgements

We thank Dr. Cova Arias (Aquatic Microbiology Laboratory, Auburn University) for helping with DNA extraction and PCR; Micah B. Warren (Aquatic Parasitology Laboratory) for help with tree building; Carlos F. Ruiz (El Paso, Texas) for helping collect myxospores of the new species; and personnel of the North Carolina Wildlife Resources Commission (Marion, North Carolina) for collecting the infected brook trout.

Funding

This project was supported by research grants from the North Carolina Wildlife Resources Commission and the Southeastern Cooperative Fish Parasite and Disease Laboratory. The findings and conclusions are those of the authors and do not necessarily represent the views of the US Fish and Wildlife Service.

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Correspondence to Steven P. Ksepka.

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Ksepka, S.P., Rash, J.M., Whelan, N. et al. A new species of Myxobolus (Myxozoa: Bivalvulida) infecting the medulla oblongata and nerve cord of brook trout Salvelinus fontinalis in southern Appalachia (New River, NC, USA). Parasitol Res 118, 3241–3252 (2019). https://doi.org/10.1007/s00436-019-06472-x

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