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Phylogeny and morphology of Ovipleistophora diplostomuri n. sp. (Microsporidia) with a unique dual-host tropism for bluegill sunfish and the digenean parasite Posthodiplostomum minimum (Strigeatida)

Published online by Cambridge University Press:  12 July 2017

J. LOVY*
Affiliation:
Office of Fish and Wildlife Health and Forensics, N.J. Division of Fish and Wildlife, 605 Pequest Road, Oxford, NJ 07863, USA
S. E. FRIEND
Affiliation:
Office of Fish and Wildlife Health and Forensics, N.J. Division of Fish and Wildlife, 605 Pequest Road, Oxford, NJ 07863, USA
*
*Corresponding author: Office of Fish and Wildlife Health and Forensics, New Jersey Division of Fish and Wildlife, 605 Pequest Road, Oxford, NJ 07863, USA. E-mail: [email protected]

Summary

Microsporidia are diverse opportunistic parasites abundant in aquatic organisms with some species hyperparasitic in digenean parasites. In the current study, we describe a unique microsporidian parasite, Ovipleistophora diplostomuri n. sp. that has a tropism for both the bluegill sunfish Lepomis macrochirus, and its digenean parasite Posthodiplostomum minimum. Though the microsporidium first infects a fish, the subsequent infection causes hypertrophy of the metacercarial wall and degeneration of the P. minimum metacercariae within the fish tissue. Genetic analysis placed this species within Ovipleistophora and ultrastructural characteristics were consistent with the genus, including the presence of dimorphic spores within sporophorous vesicles. Meronts did not have a surface coat of dense material, which has been previously reported for the genus. This is the first Ovipleistophora species described that does not have a tropism for ovary. Genetics demonstrated that O. diplostomuri n. sp. groups closely within fish microsporidia and not other species known to be hyperparasitic in digeneans, suggesting that it evolved from fish-infecting microsporidians and developed a secondary tropism for a common and widespread digenean parasite. The high genetic identity to Ovipleistophora species demonstrates the close relationship of this unique microsporidian with other microsporidia that infect ovary.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2017 

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References

REFERENCES

Barta, J. R., Martin, D. S., Liberator, P. A., Dashkevicz, M., Anderson, J. W., Feighner, S. D., Elbrecht, A., Perkins-Barrow, A., Jenkins, M. C., Danforth, H. D., Ruff, M. D. and Profous-Juchelka, H. (1997). Phylogenetic relationships among eight Eimeria species infecting domestic fowl inferred using complete small subunit ribosomal DNA sequences. Journal of Parasitology 83, 262271.CrossRefGoogle ScholarPubMed
Canning, E. U. and Madhavi, R. (1977). Studies on two new species of Microsporidia hyperparasitic in adult Allocreadium fasciatusi (Trematoda, Allocreadiidae). Parasitology 75, 293300.Google Scholar
Canning, E. U. and Nicholas, J. P. (1974). Light and electron microscope observations on Unikaryon legeri (Microsporidia, Nosematidae), a parasite of the metacercaria of Meigymnophallus minutus in Cardium edule . Journal of Invertebrate Pathology 23, 92100.Google Scholar
Canning, E. U. and Nicholas, J. P. (1980). Genus Pleistophora (Phylum Microspora): redescription of the type species, Pleistophora typicalis Gurley, 1893 and ultrastructural characterization of the genus. Journal of Fish Diseases 3, 317338.Google Scholar
Canning, E. U., Foon, L. P. and Joe, L. K. (1974). Microsporidian parasites of trematode larvae from aquatic snails in West Malaysia. Journal of Protozoology 21, 1925.Google Scholar
Canning, E. U., Barker, R. J., Hammond, J. C. and Nicholas, J. P. (1983). Unikaryon slaptonleyi sp. nov. (Microspora: Unikaryonidae) isolated from echinostome and strigeid larvae from Lymnaea peregra: observations on its morphology, transmission and pathogenicity. Parasitology 87, 175184.Google Scholar
Chapman, J. M., Marcogliese, D. J., Suski, C. D. and Cooke, S. J. (2015). Variation in parasite communities and health indices of juvenile Lepomis gibbosus across a gradient of watershed land-use and habitat quality. Ecological Indicators 57, 564572.Google Scholar
Colley, F. C., Joe, L. K., Zaman, V. and Canning, E. U. (1975). Light and electron microscopical study of Nosema eurytremae . Journal of Invertebrate Pathology 26, 1120.Google Scholar
Cort, W. W., Hussey, K. L. and Ameel, D. J. (1960a). Studies on a microsporidian hyperparasite of strigeoid trematodes. I. Prevalence and effect on the parasitized larval trematodes. Journal of Parasitology 46, 317325.Google Scholar
Cort, W. W., Hussey, K. L. and Ameel, D. J. (1960b). Studies on a microsporidian hyperparasite of strigeoid trematodes. II. Experimental transmission. Journal of Parasitology 46, 327336.Google Scholar
Crider, C. R. and Meade, T. G. (1975). Immunological studies on the origin of the cyst wall of Posthodiplostomum minimum (Trematoda: Diplostomidae). Proceedings of the Helminthological Society of Washington 42, 2124.Google Scholar
Diamant, A. and Paperna, I. (1985). The development and ultrastructure of Nosema ceratomyxae sp. nov., a microsporidian hyperparasite of the myxosporean Ceratomyxa sp. from red sea rabbitfish (Siganidae). Protistologica 21, 249258.Google Scholar
Dyková, I. (2006). Phylum Microspora. In Fish Diseases and Disorders Volume 1 Protozoan and Metazoan Infections, 2nd Edn (ed. Woo, P. T. K.), pp. 205229. CAB International, Oxfordshire, UK.Google Scholar
Felsenstein, J. (1985). Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791.Google Scholar
Ferguson, M. S. (1943). Experimental studies on the fish hosts of Posthodiplostomum minimum (Trematoda: Strigeida). Journal of Parasitology 29, 350353.Google Scholar
Freeman, M. A. and Sommerville, C. (2011). Original observations of Desmozoon lepeophtherii, a microsporidian hyperparasite infecting the salmon louse Lepeophtheirus salmonis, and its subsequent detection by other researchers. Parasites and Vectors 4, 231.Google Scholar
Grizzle, J. M. and Goldsby, M. T. Jr. (1996). White grub Posthodiplostomum minimum centrarchi metacercariae in the liver of largemouth bass: quantification and effects on health. Journal of Aquatic Animal Health 8, 7074.Google Scholar
Hall, T. A. (1999). Bioedit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 9598.Google Scholar
Hussey, K. L. (1971). A microsporidan hyperparasite of strigeoid trematodes, Nosema strigeoideae sp. n. Journal of Protozoology 18, 676679.Google Scholar
Karpov, S. A., Mamkaeva, M. A., Aleoshin, V. V., Nassonova, E., Lilje, O. and Gleason, F. H. (2014). Morphology, phylogeny, and ecology of the aphelids (Aphelidea, Opisthokonta) and proposal for the new superphylum Opisthosporidia. Frontiers in Microbiology 5, 112.Google Scholar
Kent, M. L., Shaw, R. W. and Sanders, J. L. (2014). Microsporidia in fish. In Microsporidia: Pathogens of Opportunity, 1st Edn (ed. Weiss, L. M. and Becnel, J. J.), Ch20, John Wiley and Sons, Inc., Chichester, UK.Google Scholar
Kimura, M. (1980). A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.Google Scholar
Klak, G. (1940). Neascus infestation of black-head, blunt-nosed, and other forage minnows. Transactions of the American Fisheries Society 69, 273278.CrossRefGoogle Scholar
Kumar, S., Stecher, G. and Tamura, K. (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33, 18701874.Google Scholar
Lane, B., Spier, T., Wiederholt, J. and Meagher, S. (2015). Host specificity of a parasitic fluke: is Posthodiplostomum minimum a centrarchid-infecting generalist or specialist? Journal of Parasitology 101, 617.CrossRefGoogle ScholarPubMed
Levron, C., Ternengo, S., Toguebaye, B. S. and Marchand, B. (2004). Ultrastructural description of the life cycle of Nosema diphterostomi sp. n., a microsporidia hyperparasite of Diphterostomum brusinae (Digenea: Zoogonidae), intestinal parasite of Diplodus annularis (Pisces: Teleostei). Acta Protozoologica 43, 329336.Google Scholar
Levron, C., Ternengo, S., Toguebaye, B. S. and Marchand, B. (2005). Ultrastructural description of the life cycle of Nosema monorchis n. sp. (Microspora, Nosematidae), hyperparasite of Monorchis parvus (Digenea, Monorchiidae), intestinal parasite of Diplodus annularis (Pisces, Teleostei). European Journal of Protistology 41, 251256.CrossRefGoogle Scholar
Lewis, W. M. and Nickum, J. (1964). The effect of Posthodiplostomum minimum upon the body weight of the bluegill. The Progressive Fish-Culturist 26, 121123.Google Scholar
Li, K., Chang, O., Wang, F., Liu, C., Liang, H. and Wu, S. (2012) Ultrastructure, development, and molecular phylogeny of Pleistophora hyphessobryconis, a broad host microsporidian parasite of Puntius tetrazona . Parasitology Research 111, 17151724.Google Scholar
Lom, J. (2002). A catalogue of described genera and species of microsporidians parasitic in fish. Systematic Parasitology 53, 8199.Google Scholar
Lom, J. and Nilsen, F. (2003). Fish microsporidia: fine structural diversity and phylogeny. International Journal for Parasitology 33, 107127.Google Scholar
Maurand, J., Loubes, C., Gasc, C., Pelletier, J. and Barral, J. (1988). Pleistophora mirandellae Vaney & Conte, 1901, a microsporidian parasite in cyprinid fish of rivers in Hérault: taxonomy and histopathology. Journal of Fish Diseases 11, 251258.Google Scholar
Miller, J. H. (1954). Studies on the life history of Posthodiplostomum minimum (MacCallum 1921). Journal of Parasitology 40, 255270.Google Scholar
Mitchell, A. J., Smith, C. E. and Hoffman, G. L. (1982). Pathogenicity and histopathology of an unusually intense infection of white grubs (Posthodiplostomum m. minimum) in the fathead minnow (Pimephales promelas). Journal of Wildlife Diseases 18, 5157.Google Scholar
Mitchell, C. W. (1974). Ultrastructure of the metacercarial cyst of Posthodiplostomum minimum (MacCallum, 1921). Journal of Parasitology 60, 6774.Google Scholar
Nei, M. and Kumar, S. (2000). Molecular Evolution and Phylogenetics. Oxford University Press, New York, USA.Google Scholar
Nylund, S., Nylund, A., Watanabe, K., Arnesen, C. E. and Karlsbakk, E. (2010). Paranucleospora theridion n. gen., n. sp. (Microsporidia, Enterocytozoonidae) with a life cycle in the salmon louse (Lepeophtheirus salmonis, Copepoda) and Atlantic salmon (Salmo salar). Journal of Eukaryotic Microbiology 57, 95114.Google Scholar
Nylund, S., Anderson, L., Saevareid, I., Plarre, H., Watanabe, K., Arnesen, C. E., Karlsbakk, E. and Nylund, A. (2011). Diseases of farmed Atlantic salmon Salmo salar associated with infections by the microsporidian Paranucleospora theridion . Diseases of Aquatic Organsims 94, 4157.Google Scholar
Palmieri, J. R. (1975). Physiological strains of the strigeoid trematode, Posthodiplostomum minimum (Trematoda: Diplostomatidae). Journal of Parasitology 61, 1107.Google Scholar
Paperna, I. and Dzikowski, R. (2006). Digenea (Phylum Platyhelminthes). In Fish Diseases and Disorders Volume 1 Protozoan and Metazoan Infections, 2nd Edn (ed. Woo, P. T. K.), pp. 345390. CAB International, Oxfordshire, UK.Google Scholar
Paperna, I., Sabnai, I. and Castel, M. (1978). Microsporidian infection in the cyst wall of trematode metacercariae encysted in fish. Annales de parasitologie humaine et comparée 53, 123130.Google Scholar
Pekkarinen, M., Lom, J. and Nilsen, F. (2002). Ovipleistophora gen. n., a new genus for Pleistophora mirandellae-like microsporidia. Diseases of Aquatic Organisms 48, 133142.Google Scholar
Ruehl-Fehlert, C., Bomke, C., Dorgerloh, M., Palazzi, X. and Rosenbruch, M. (2005). Pleistophora infestation in fathead minnows, Pimephales promelas (Rafinesque). Journal of Fish Diseases 28, 629637.Google Scholar
Sanders, J. L., Lawrence, C., Nichols, D. K., Brubaker, J. F., Peterson, T. S., Murray, K. N. and Kent, M. L. (2010). Pleistophora hyphessobryconis (Microsporidia) infecting zebrafish Danio rerio in research facilities. Diseases of Aquatic Organisms 91, 4756.Google Scholar
Sene, A., Ba, C. T., Marchand, B. and Toguebaye, B. S. (1997). Ultrastructure of Unikaryon nomimoscolexi n. sp. (Microsporidia, Unikaryonidae), a parasite of Nomimoscolex sp. (Cestoda, Proteocephalidea) from the gut of Clarotes laticeps (Pisces, Teleostei, Bagridae). Diseases of Aquatic Organisms 29, 3540.Google Scholar
Sprague, V. (1964). Nosema dollfusi n. sp. (Microsporidia, Nosematidae), a hyperparasite of Bucephalus cuculus in Crassostrea virginica . Journal of Eukaryotic Microbiology 11, 381385.Google Scholar
Sprague, V. (1977). Annotated list of species of microsporidia. In Comparative Pathobiology Volume 2 Systematics of the Microsporidia (ed. Bulla, L. A. and Cheng, T. C.), pp. 31334. Plenum Press, New York, USA.Google Scholar
Stentiford, G. D., Feist, S. W., Stone, D. M., Bateman, K. S. and Dunn, A. M. (2013). Microsporidia: diverse, dynamic, and emergent pathogens in aquatic systems. Trends in Parasitology 29, 567578.Google Scholar
Stentiford, G. D., Ramilo, A., Abollo, E., Kerr, R., Bateman, K. S., Feist, S. W., Bass, D. and Villalba, A. (2017). Hyperspora aquatica n. gn., n. sp. (Microsporidia), hyperparasitic in Marteilia cochillia (Paramyxida), is closely related to crustacean-infecting microsporidian taxa. Parasitology 144, 186199.Google Scholar
Summerfelt, R. C. and Goodwin, A. E. (2010). Ovipleistophoriasis: a microsporidian disease of the golden shiner ovary. In American Fisheries Society-Fish Health Section Blue Book: Suggested Procedures for the Detection and Identification of Certain Finfish and Shellfish Pathogens, 1.3.2.3, 2016 edition. Accessible at: http://afs-fhs.org/bluebook/bluebook-index.php.Google Scholar
Sveen, S., Overland, H., Karlsbakk, E. and Nylund, A. (2012). Paranucleospora theridion (Microsporidia) infection dynamics in farmed Atlantic salmon Salmo salar put to sea in spring and autumn. Diseases of Aquatic Organisms 101, 4349.Google Scholar
Toguebaye, B. S., Quilichini, Y., Diagne, P. M. and Marchand, B. (2014). Ultrastructure and development of Nosema podocotyloidis n. sp. (Microsporidia), a hyperparasite of Podocotyloides magnatestis (Trematoda), a parasite of Parapristipoma octolineatum (Teleostei). Parasite 21, 44.Google Scholar
Vossbrinck, C. R., Baker, M. D., Didier, E. S., Debrunner-Vossbrinck, B. A. and Shadduck, J. A. (1993). Ribosomal DNA sequences of Encephalitozoon hellem and Encephalitozoon cuniculi: species identification and phylogenetic construction. Journal of Eukaryotic Microbiology 40, 354362.Google Scholar
Vossbrinck, C. R., Andreadis, T. G., Vavra, J. and Becnel, J. J. (2004). Molecular phylogeny and evolution of mosquito parasitic microsporidia (Microsporidia: Amblyosporidae). Journal of Eukaryotic Microbiology 51, 8895.Google Scholar
Williams, B. A., Haferkamp, I. and Keeling, P. J. (2008). An ADP/ATP-specific mitochondrial carrier protein in the microsporidian Antonospora locustae . Journal of Molecular Biology 375, 12491257.Google Scholar
Winters, A. D., Langohr, I. M., Souza, M. D., Colodel, E. M., Soares, M. P. and Faisal, M. (2016). Ultrastructure and molecular phylogeny of Pleistophora hyphessobryconis (Microporidia) infecting hybrid jundiara (Leiarius marmoratus×Pseudoplatystoma reticulatum) in a Brazilian aquaculture facility. Parasitology 143, 4149.Google Scholar