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A morphological, molecular, and histopathological redescription of Henneguya nyongensis Fomena & Bouix, 1996 (Cnidaria: Myxobolidae) infecting the gills of Peter’s elephantnose fish, Gnathonemus petersii (Günther) (Osteoglossiformes: Mormyridae), imported from Nigeria

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Abstract

A Henneguya sp., morphologically resembling Henneguya nyongensis Fomena & Bouix, 1996, was isolated from the gills of Peter’s elephantnose fish, Gnathonemus petersii Günther, imported from Nigeria. Plasmodia were located between lamellae and within the gill epithelium, often leading to lamellar fusion. Although slightly smaller, the myxospores from these fish were morphologically consistent with H. nyongensis. In valvular view, spores are elongate, pyriform with a rounded posterior and tapering caudal processes. Myxospore bodies are 9.6–12.3 (mean 11.2) µm long and 4.0–4.7 (mean 4.3) µm wide. Polar capsules are pyriform, elongate, 4.5–5.2 (4.7) µm long and 1.3–1.6 (1.4) µm wide, with a characteristic neck-like structure at the apical end. Sequence generated for the 18S small subunit rRNA gene did not directly match any sequences available on GenBank, but demonstrated 91% nucleotide similarity to an unpublished Henneguya sp. infecting Mormyrus kannume Forsskål. Herein, the description of H. nyongensis is supplemented with new data on histopathology, molecular characterisation, and expanded host and geographical range.

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References

  • Alama-Bermejo, G., Jirků, M., Kodádková, A., Pecková, H., Fiala, I., & Holzer, A. S. (2016). Species complexes and phylogenetic lineages of Hoferellus (Myxozoa, Cnidaria) including revision of the genus: A problematic case for taxonomy. Parasites & Vectors,9, 13.

    Article  Google Scholar 

  • Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology,215, 403–410.

    Article  CAS  Google Scholar 

  • Barta, J. R., Marin, D. S., Liberator, P. A., Dshkevicz, M., Anderson, J. W., Feighner, S. D., et al. (1997). Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology,83, 262–271.

    Article  CAS  Google Scholar 

  • Bellerud, B. L., Pote, L. M., Lin, T. L., Johnson, M. J., & Boyle, C. R. (1995). Etiological and epizootological factors associated with outbreaks of proliferative gill disease in channel catfish. Journal of Aquatic Animal Health,7, 124–131.

    Article  Google Scholar 

  • Caffara, M., De Vita, V., Florio, D., Gustinelli, A., Quaglio, F., & Fioravanti, M. L. (2007). Infections due to Unicauda spp. (Myxozoa, Myxobolidae) in elephantnose fish (Gnathonemus petersii) imported to Italy. Bulletin of the European Association of Fish Pathologists,27, 142–147.

    Google Scholar 

  • Declercq, A. M., Haesebrouck, F., Van den Broeck, W., Bossier, P., & Decostere, A. (2013). Columnaris disease in fish: A review with emphasis on bacterium-host interactions. Veterinary Research,44, 27.

    Article  Google Scholar 

  • Dohle, A., Schmahl, G., Raether, W., Schmidt, H., & Ritter, G. (2002). Effects of orally administered chemotherapeutics (quinine, salinomycin) against Henneguya sp. Thélohan, 1892 (Myxozoa: Myxobolidae), a gill parasite in the tapir fish Gnathonemus petersii Gunther, 1862 (Teleostei). Parasitology Research,88, 861–867.

    Article  Google Scholar 

  • Fevre, E. M., Bronsvoort, B. M., Hamilton, K. A., & Cleaveland, S. (2006). Animal movements and the spread of infectious diseases. Trends in Microbiology,14, 125–131.

    Article  CAS  Google Scholar 

  • Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution,39, 783–791.

    Article  Google Scholar 

  • Fiala, I., Bartošová-Sojková, P., & Whipps, C. M. (2015). Classification and phylogenetics of Myxozoa. In: Okamura, B., Gruhl, A. & Bartholomew, J. L. (Eds), Myxozoan evolution, ecology and development. Cham: Springer. pp. 85–110.

    Chapter  Google Scholar 

  • Fomena, A., & Bouix, G. (1994). New Myxosporidea species (Myxozoa) from freshwater teleosts in southern Cameroon (Central Africa). Journal of African Zoology,108, 481–491.

    Google Scholar 

  • Fomena, A., & Bouix, G. (1996). New species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea) parasites of freshwater fishes in Cameroon. Journal of African Zoology,110, 413–423.

    Google Scholar 

  • Go, J., Lancaster, M., Deece, K., Dhungyel, O., & Whittington, R. (2006). The molecular epidemiology of iridovirus in Murray cod (Maccullochella peelii peelii) and dwarf gourami (Colisa lalia) from distant biogeographical regions suggests a link between trade in ornamental fish and emerging iridoviral diseases. Molecular & Cellular Probes,20, 212–222.

    Article  CAS  Google Scholar 

  • Griffin, M. J., Pote, L. M., Wise, D. J., Greenway, T. E., Mauel, M. J., & Camus, A. C. (2008). A novel Henneguya species from channel catfish described by morphological, histological and molecular characterization. Journal of Aquatic Animal Health,20, 127–135.

    Article  CAS  Google Scholar 

  • Hallett, S. L., Atkinson, S. D., Erseus, C., & El-Matbouli, M. (2005). Dissemination of triactinomyxons (Myxozoa) via oligochaetes used as live food for aquarium fishes. Diseases of Aquatic Organisms,65, 137–152.

    Article  Google Scholar 

  • Hallett, S. L., & Diamant, A. (2001). Ultrastructure and small-subunit ribosomal DNA sequence of Henneguya lesteri n. sp. (Myxosporea), a parasite of sand whiting Sillago analis (Sillaginidae) from the coast of Queensland. Australia. Diseases of Aquatic Organisms,46, 197–212.

    Article  CAS  Google Scholar 

  • Hanson, L. A., Lin, D., Pote, L. M., & Shivaji, R. (2001). Small subunit rRNA gene comparisons of four actinosporean species to establish a polymerase chain reaction test for the causative agent of proliferative gill disease in channel catfish. Journal of Aquatic Animal Health,13, 117–123.

    Article  Google Scholar 

  • Hedrick, R. P., Wishkovsky, A., Modin, J. C., & Toth, R. J. (1991). Three myxosporeans found in the cranial and branchial tissues of rainbow trout in California. Journal of Aquatic Animal Health,3, 55–62.

    Article  Google Scholar 

  • Katoh, K., Misawa, K., Kuma, K., & Miyata, T. (2002). MAFFT: A novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research,30, 3059–3066.

    Article  CAS  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution,30, 772–780.

    Article  CAS  Google Scholar 

  • Kent, M. L., Khattra, J., Hedrick, R. P., & Devlin, R. H. (2000). Tetracapsula renicola n. sp. (Myxozoa: Saccosporidae); the PKX myxozoan - the cause of proliferative kidney disease of salmonid fishes. Journal of Parasitology,86, 103–111.

    CAS  PubMed  Google Scholar 

  • Kostoïngue, B., Diebakate, C., Faye, N., & Toguebaye, B. S. (2001). Presence of Myxosporidea (Myxozoa: Myxosporea) of the genus Henneguya Thélohan in freshwater fishes from Chad (Central Africa). Acta Protozoologica,40, 117–123.

    Google Scholar 

  • Kumar, S., Stecher, G., & Tamura, K. (2016). MEGA7: Molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution,33, 1870–1874.

    Article  CAS  Google Scholar 

  • Lom, J., & Arthur, M. C. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases,12, 151–156.

    Article  Google Scholar 

  • Mrugala, A., Kozubikova-Balcarova, E., Chucholl, C., Cabanillas Resino, S., Viljamaa-Dirks, S., Vukic, J., et al. (2015). Trade of ornamental crayfish in Europe as a possible introduction pathway for important crustacean disease: crayfish plague and white spot syndrome. Biological Invasions,17, 1313–1326.

    Article  Google Scholar 

  • Nei, M., & Kumar, S. (2000). Molecular evolution and phylogenetics. New York: Oxford University Press.

    Google Scholar 

  • Noga, E. J. (2010). Fish disease diagnosis and treatment. Ames, IA: Wiley-Blackwell.

    Book  Google Scholar 

  • Parker, J. D., & Warner, M. C. (1970). Effects of fixation, dehydration, and staining on dimensions of myxosporidian and microsporidian spores. Journal of Wildlife Diseases,6, 448–456.

    Article  CAS  Google Scholar 

  • Peeler, E. J., Oidtmann, B. C., Midtlyng, P. J., Miossec, L., & Gozlan, R. E. (2011). Non-native aquatic animals introductions have driven disease emergence in Europe. Biological Invasions,13, 1291–1303.

    Article  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics,19, 1571–1574.

    Article  Google Scholar 

  • Rosser, T. G., Khoo, L. H., Pote, L. M., & Griffin, M. J. (2016). Verrucous dermal henneguyosis associated with Henneguya exilis (Kudo, 1929) (Cnidaria: Myxobolidae), a parasite of the channel catfish Ictalurus punctatus (Rafinesque, 1818). Journal of Fish Diseases,39, 1263–1267.

    Article  CAS  Google Scholar 

  • Schmahl, G., Senaud, J., & Mehlhorn, H. (1991). Treatment of fish parasites 8. Effects of sym. Triazinone (toltrazuril) on developmental stages of Henneguya sp. (Myxozporea, Myxozoa): a light and electron microscopic study. Archiv für Protistenkunde,140, 83–94.

    Article  Google Scholar 

  • Stilwell, J. M., Camus, A. C., Leary, J. H., Khoo, L. H., & Griffin, M. J. (2019). Pathologic changes associated with respiratory compromise and morbidity due to massive interlamellar Henneguya exilis infection in channel × blue hybrid catfish. Journal of Parasitology,105, 686–692.

    Article  Google Scholar 

  • Trujillo-Gonzalez, A., Becker, J. A., & Hutson, K. S. (2018). Parasite dispersal from the ornamental goldfish trade. Advances in Parasitology,100, 239–281.

    Article  Google Scholar 

  • Wagner, E. J. (2016). A Guide to the identification of tailed Myxobolidae of the world: Dicauda, Hennegoides, Henneguya, Laterocapsulata, Neohenneguya, Phlogospora, Tetrauronema, Trigonosporus, and Unicauda. Logan, Utah: Fish Creek Records.

    Google Scholar 

  • Whittington, R. J., & Chong, R. (2007). Global trade in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Preventive Veterinary Medicine,81, 92–116.

    Article  CAS  Google Scholar 

  • Wise, D. J., Camus, A. C., Schwedler, T. E., & Terhune, J. S. (2004). Health management. In: Tucker, C. S. & Hargreaves, J. A. (Eds), Biology and culture of channel catfish (pp. 444–498). Amsterdam: Elsevier B. V.

    Chapter  Google Scholar 

  • Wise, D. J., Griffin, M. J., Terhune, J. S., Pote, L. M., & Khoo, L. H. (2008). Induction and evaluation of proliferative gill disease in channel catfish fingerlings. Journal of Aquatic Animal Health,20, 236–244.

    Article  Google Scholar 

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Correspondence to Justin M. Stilwell.

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Stilwell, J.M., Stilwell, N.K., Camus, A.C. et al. A morphological, molecular, and histopathological redescription of Henneguya nyongensis Fomena & Bouix, 1996 (Cnidaria: Myxobolidae) infecting the gills of Peter’s elephantnose fish, Gnathonemus petersii (Günther) (Osteoglossiformes: Mormyridae), imported from Nigeria. Syst Parasitol 96, 767–776 (2019). https://doi.org/10.1007/s11230-019-09887-3

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