Abstract
Henneguya Thélohan, 1892 is the second most species rich genus of myxozoans, with reports from freshwater and marine fish worldwide. In the Great Lakes region of North America, muskellunge Esox masquinongy is an important game fish species that serves as an apex predator in the ecosystems of many inland lakes. The myxozoan fauna of esocid fish, especially muskellunge, remains largely understudied. During fish health assessments, muskellunge were examined for parasitic infections and myxozoan pseudocysts were observed on gill clip wet mounts. When ruptured under pressure, the intralamellar pseudocysts released thousands of myxospores consistent with those of the genus Henneguya. The myxospores were 67.3–96.6 (79.1 ± 5.9) µm in total length. The spore body was 18.6–22.6 (20.9 ± 1.0) µm × 5.4–6.9 (6.3 ± 0.4) µm in valvular view and 3.5–4.0 (3.8 ± 0.3) µm wide in sutural view. The two pyriform polar capsules positioned at the anterior of the spore body were 6.4–7.7 (7.0 ± 0.4) µm × 1.8–2.1 (2.0 ± 0.1) µm and each contained a tightly coiled polar filament with 9–10 turns. Two tapering caudal processes extended from the posterior of the spore body and were 47.3–75.6 (58.3 ± 5.8) µm in length. Histologically, large intralamellar polysporic plasmodia were surrounded by plump pillar cells and a distinct layer of plasma. Mild inflammation was present peripherally, with small numbers of necrotic germinative cells and intraplasmodial phagocytes internally. Ribosomal 18S rRNA gene sequence data were obtained from three gill pseudocysts. The three ~2000-bp sequences were identical, but shared no significant similarity with any publicly available sequence data. Phylogenetic analyses demonstrated sequence data from this Henneguya fell within a well-supported clade of Henneguya spp. reported from northern pike Esox lucius in Europe. Based on the distinct morphological, histological and molecular data, this species is designated as Henneguya michiganensis n. sp. from muskellunge in Michigan, USA.
Similar content being viewed by others
References
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.
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.
Bond, F. F. (1939). Myxosporidia from fishes of the genus Esox. Journal of Parasitology, 25, 377–381.
Cohn, L. (1896). Ueber die Myxosporidien von Esox lucius und Perca flviatilis. Zoologische Jahrbücher, Abteilung für Anatomie, 9, 229–272.
Crane, D. P., Miller, L. M., Diana, J. S., Casselman, J. M., Farrell, J. M., Kapuscinski, K. L., et al. (2015). Muskellunge and Northern Pike ecology and management: important issues and research needs. Fisheries, 40, 258–267.
Current, W. L., & Janovy, J. (1978). Comparative study of ultrastructure of interlamellar and intralamellar types of Henneguya exilis Kudo from channel catfish. Journal of Protozoology, 25, 56–65.
Dyková, I., & Lom, J. (1978). Histopathological changes in fish gills infected with myxosporidian parasites of the genus Henneguya. Journal of Fish Biology, 12, 197–202.
Elsayed, E., Faisal, M., Thomas, M., Whelan, G., Batts, W., & Winton, J. (2006). Isolation of viral haemorrhagic septicaemia virus from muskellunge, Esox masquinongy (Mitchill), in Lake St Clair, Michigan, USA reveals a new sublineage of the North American genotype. Journal of Fish Diseases, 29, 611–619.
Fantham, H. B., Porter, A., & Richardson, L. R. (1939). Some Myxosporidia found in certain freshwater fishes in Quebec province, Canada. Parasitology, 31, 1–77.
Faisal, M., Baird, A., Winters, A. D., Millard, E. V., Marcquenski, S., Hsu, H. M., et al. (2016a). Isolation of the fathead minnow nidovirus from muskellunge experiencing lingering mortality. Journal of Aquatic Animal Health, 28, 131–141.
Faisal, M., Diamanka, A., Loch, T., Lafrentz, B., Winters, A., Garcia, J., et al. (2016b). Isolation and characterization of Flavobacterium columnare strains infecting fishes inhabiting the Laurentian Great Lakes basin. Journal of Fish Diseases, 40, 637–648.
Fiala, I., Bartošová-Sojková, P., & Whipps, C. M. (2015). Classification and phylogenetics of Myxozoa. In: B. Okamura, A. Gruhl, & J. L. Bartholomew (Eds.), Myxozoan Evolution, Ecology and Development (pp. 85–110). Cham, Switzerland: Springer International Publishing.
Ganapati, P. N. (1941). On a new Myxosporidian Henneguya otolithi n. sp. a tissue parasite from the bulbus arteriosus of two species of fish of the genus Otolithus. Proceedings: Plant Sciences, 13, 135–150.
Gómez, D., Bartholomew, J., & Sunyer, J. O. (2014). Biology and mucosal immunity to myxozoans. Developmental & Comparative Immunology, 43, 243–256.
Grassé, P.-P., & Lavette, A. (1978). Myxosporidia Sphaeromyxa sabrazesi and new embranchment of Myxozoa - researches upon pluricellular stage and considerations of phylogeny. Annales des sciences Naturelles Zoologie et Biologie Animale, 20, 193–285.
Griffin, M. J., Camus, A. C., Wise, D. J., Greenway, T. E., Mauel, M. J., & Pote, L. M. (2010). Variation in susceptibility to Henneguya ictaluri infection by two species of catfish and their hybrid cross. Journal of Aquatic Animal Health, 22, 21–35.
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.
Guilford, H. G. (1965). New species of Myxosporidia from Green Bay (Lake Michigan). Transactions of the American Microscopical Society, 84, 566–573.
Gurley, R. R. (1894). The Myxosporidia or psorosperms of fishes, and the epidemics produced by them. Reports of the United States Fish Commission, 26, 65–304.
Hallett, S. L., & Diamant, A. (2001). Ultrastrucutre 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.
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.
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.
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.
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.
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.
Leis, E. M., Rosser, T. G., Baumgartner, W. A., & Griffin, M. J. (2017). Henneguya laseeae n. sp. from flathead catfish (Pylodictis olivaris) in the upper Mississippi River. Parasitology Research, 116, 81–89.
Lom, J., & Arthur, J. R. (1989). A guideline for the preparation of species description in Myxosporea. Journal of Fish Diseases, 12, 151–156.
Lom, J., & Dyková, I. (1992). Protozoan Parasites of Fishes. New York: Elsevier.
Lom, J., & Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53, 1–36.
Minchew, C. D. (1977). Five new species of Henneguya (Protozoa: Myxosporida) from ictalurid fishes. Journal of Protozoology, 24, 213–220.
Molnár, K. (1998). Taxonomic problems, seasonality and histopatholoyg of Henneguya creplini (Myxosporea) infection of the pikeperch Stizostedion lucioperca in Lake Balaton. Folia Parasitologica, 45, 261–269.
Molnár, K. (2002). Site preference of fish myxosporeans in the gill. Diseases of Aquatic Organisms, 48, 197–207.
Naldoni, J., Arana, S., Maia, A. A. M., Ceccarelli, P. S., Tavares, L. E. R., Borges, F. A., et al. (2009). Henneguya pseudoplatystoma n. sp. causing reduction in epithelial area of gills in the farmed pintado, a South American catfish: histopathology and ultrastructure. Veterinary Parasitology, 166, 52–59.
Nei, M., & Kumar, S. (2000). Molecular Evolution and Phylogenetics. New York: Oxford University Press.
Phillips, K., Noyes, A., Shen, L. & Whelan, G. (2014). Model program for fish health management in the Great Lakes. In: Great Lakes Fishery Commision Special Publication 14-02.
Pote, L. M. W., Khoo, L., & Griffin, M. (2012). Henneguya ictaluri. In P. T. K. Woo & K. Bachman, Fish Parasites: Pathobiology and Protection (pp. 177–192). Cambridge, MA, USA: CAB International.
Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19, 1571–1574.
Rosser, T. G., Khoo, L. H., Wise, D. J., Mischke, C. C., Greenway, T. E., Alberson, N. R., et al. (2019). Arrested development of Henneguya ictaluri (Cnidaria: Myxobolidae) in ♀ channel catfish × ♂ blue catfish hybrids. Journal of Aquatic Animal Health, 31, 201–213.
Rosser, T. G., Griffin, M. J., Quiniou, S. M., Khoo, L. H., Greenway, T. E., Wise, D. J., et al. (2015). Small subunit ribosomal RNA sequence links the myxospore stage of Henneguya mississippiensis n. sp. from channel catfish Ictalurus punctatus to an actinospore released by the benthic oligochaete Dero digitata. Parasitology Research, 114, 1595–1602.
Rosser, T. G., Griffin, M. J., Quiniou, S. M., Khoo, L. H., & Pote, L. M. (2014). 18S rRNA gene sequencing identifies a novel species of Henneguya parasitizing the gills of the channel catfish (Ictaluridae). Parasitology Research, 113, 4651–4658.
Shariff, M. (1982). Henneguya shaharini sp. nov. (Protozoa: Myxozoa), a parasite of marble goby, Oxyeleotns marmoratus (Bleeker). Journal of Fish Diseases, 5, 37–45.
Smith, K. M., Thomas, M. V., & Hanchin, P. A. (2016). Management plan for muskellunge in Michigan. In: Michigan Department of Natural Resources Fisheries Report. Michigan Department of Natural Resources, Lansing.
Speare, D. J., & Ferguson, H. W. (2006). Gills and pseudobranchs. In: H. W. Ferguson (Ed.), Systemic Pathology of Fish: a text and atlas of normal tissues in teleosts and their responses in disease (pp. 24–62). London: Scotian.
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.
Thélohan, P. (1892). Observation sur les myxosporidies et éssai de classification de ces organisms. Bulletin de la Société Philomatique, 4, 165–178.
Webb, S. R., Garman, G. C., McIninch, S. P., Nerad, T. A., Peglar, M. T., Gillevet, P. M., et al. (2005). Etiology of ulcerative lesions of Atlantic menhaden (Brevoortia tyrannus) from James River, Virginia. Parasitology Research, 97, 358–366.
Yokoyama, H., Kawakami, H., Yasuda, H., & Tanaka, S. (2003). Henneguya lateolabracis n. sp. (Myxozoa: Myxosporea), the causative agent of cardiac henneguyosis in Chinese sea bass Lateolabrax sp. Fisheries Science, 69, 1116–1120.
Acknowledgements
The authors thank Michigan Department of Natural Resources personnel for fish collections, particularly Mr. Todd Summers and Mr. Matt Hughes. The authors also thank past and present members of the Michigan State University – Aquatic Animal Health Laboratory for technical assistance.
Funding
This research was supported by the Michigan Department of Natural Resources and the Mississippi State University College of Veterinary Medicine.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical approval
All applicable institution, national and international guidelines for the care and use of animals were followed. All fish handling and processing was performed in accordance with Michigan State University Institutional Animal Care and Use Committee (IACUC) standards (AUF 07/12-124-99).
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
This article was registered in the Official Register of Zoological Nomenclature (ZooBank) as urn:lsid:zoobank.org:pub:6E88B072-457F-46C6-8E6A-B23E2CBE8D07. This article was published as an Online First article on the online publication date shown on this page. The article should be cited by using the doi number. This is the version of record.
Rights and permissions
About this article
Cite this article
Rosser, T.G., Loch, T.P., Faisal, M. et al. Henneguya michiganensis n. sp. (Cnidaria: Myxosporea) from the gills of muskellunge Esox masquinongy Mitchill(Esociformes: Esocidae). Syst Parasitol 98, 119–130 (2021). https://doi.org/10.1007/s11230-021-09965-5
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11230-021-09965-5