Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter July 4, 2018

Morphological and phylogenetic characterization of a novel Unicauda species, infecting the kidney of Astyanax altiparanae (Teleostei: Characidae) in Brazil

Letícia P. Vidal, Douglas McIntosh and José L. Luque
From the journal Acta Parasitologica

Abstract

During a parasitological survey of Astyanax altiparanae captured in the Mogi Guaçú river, Pirassununga, state of São Paulo, Brazil, a new species of myxozoa was observed infecting the kidney of 30 of 42 specimens. Plasmodia of the new myxozoa, referred to herein as Unicauda whippsi n. sp. were spherical and varied from 450 to 1000 μm in length. The mature spore was elongated and measured 11 ± 1.2 (10–12) μm long by 5.4 ± 0.6 (4.7–7.2) μm wide. Polar capsules of unequal length with the filament coiled 7–9 times and a unique caudal process characteristic of the genus Unicauda, were recorded. Phylogenetic analysis demonstrated that U. whippsi n. sp. clustered with members of the genus Unicauda and Myxobolus, confirming it’s placement within the family Myxobolidae. This is the first record of a species of Unicauda infecting characiform fish, as well as the first registered occurrence of species of this genus in South America.

Acknowledgements

To Dr. Júlio Cesar C. de Aguiar (CEPTA/ICM-Bio) for assistance in the development of the work. Letícia G. P. Vidal was supported by a Postdoctoral fellowship from PNPD-CAPES (Programa Nacional de Pós-Doutorado-Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) and José L. Luque was supported by a Researcher fellowship from CNPq.

References

Andree A.K.B., Székely C., Molnár K., Gresoviac S. J., Hedrick R.P. 1999. Relationships among members of the Genus Myxobolus (Myxozoa: Bivalvulidea) based on small subunit ribosomal DNA sequence. Journal of Parasitology, 85, 68–74. 10.2307/3285702Search in Google Scholar

Azevedo C., Rocha S., Matos P., Matos E., Oliveira E., Al-Quraishy S., Casal G. 2014. Morphology and phylogeny of Henneguya jocu n. sp. (Myxosporea, Myxobolidae), infecting the gills of the marine fish Lutjanus jocu. European Journal of Protistology, 50, 185–193. 10.1016/j.ejop.2013.12.002Search in Google Scholar

Bahri S., Andree K.B., Hedrick R.P. 2003. Morphological and phylogenetic studies of marine Myxobolus spp. from mullet in Ichkeul Lake, Tunisia. Journal of Eukaryotic Microbiology, 50, 463–470. 10.1111/j.1550-7408.2003.tb00272.xSearch in Google Scholar

Bahri S., Marton S., Marques A., Eszterbauer E. 2010. Henneguya tunisiensis n. sp. (Myxosporea: Bivalvulida), a new gill parasite of Symphodus tinca (L.) (Teleostei: Labridae) off Tunisia. Systematic Parasitology, 76, 93–101. 10.1007/s11230-010-9237-zSearch in Google Scholar

Barassa, B., Cordeiro, N.S., Arana, S. 2003. A new species of Henneguya, a gill parasite of Astyanax altiparanae (Pisces: Characidae) from Brazil, with comments on histopathology and seasonality. Memórias do Instituto Oswaldo Cruz, 98, 761–765. 10.1590/S0074-02762003000600009Search in Google Scholar

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 D., Ruff M.D., 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, 262–271. 10.2307/3284453Search in Google Scholar

Baska F., Voronin V.N., Eszterbauer E., Müller L., Marton S., Molnár K. 2009. Occurrence of two myxosporean species, Myxobolus hakyi sp. n. and Hoferellus pulvinatus sp. n., in Pangasianodon hypophthalmus fry imported from Thailand to Europe as ornamental fish. Parasitology Research, 105, 1391–1398. 10.1007/s00436-009-1567-xSearch in Google Scholar

Camus A.C., Dill J.A., Rosser T.G., Pote L.M., Griffin M.J. 2017. Myxobolus axelrodi n. sp. (Myxosporea: Myxobolidae) a parasite infecting the brain and retinas of the cardinal tetra Paracheirodon axelrodi (Teleostei: Characidae). Parasitology Research, 116, 387–397. 10.1007/s00436-016-5301-1Search in Google Scholar

Canning E. U., Okamura B. 2004. Biodiversity and Evolution of the Myxozoa. Advances in Parasitology, 56, 43–131. 10.1016/S0065-308X(03)56002-XSearch in Google Scholar

Capodifoglio K.R.H., Adriano E.A., Milanin T., Silva M.R.M., Maia A.A.M. 2016. Morphological, ultrastructural and phylogenetic analyses of Myxobolus hilarii n. sp. (Myxozoa, Myxosporea), a renal parasite of farmed Brycon hilarii in Brazil. Parasitology International, 65, 184–190. 10.1016/j.parint.2015.12.006Search in Google Scholar PubMed

Capodifoglio K.R.H., Adriano E.A., Silva M.R.M., Maia A.A.M. 2015. Supplementary data of Henneguya leporinicola (Myxozoa, Myxosporea) a parasite of Leporinus macrocephalus from fish farms in the state of São Paulo, Brazil. Acta Parasitologica, 60, 451–458. 10.1515/ap-2015-0062Search in Google Scholar PubMed

Carriero M.M., Adriano E.A., Silva M.R.M., Ceccarelli P.S., Maia A.A.M., 2013. Molecular phylogeny of the Myxobolus and Henneguya genera with several new South American species. PLoS One, 8, e73713. 10.1371/j0073713Search in Google Scholar

Chen C., MA C. 1998. Fauna Sinica. Myxozoa. Myxosporea. Science Press, Beijing, 292–528. (In Chinese)Search in Google Scholar

Cone D.K., Melendy J.S. 2000. Infections of Unicauda clavicauda (Kudo 1933) (Myxozoa) in the skin of Notropis hudsonius (Cyprinidae) from Montana, with a synopsis of the genus Unicauda Davis, 1944. Folia Parasitologica, 47, 273–278. 10.14411/fp.2000.047Search in Google Scholar PubMed

Darriba D., Taboada G.L., Ramón D., Posada D. 2012. jModelTest 2: more models, new heuristics and high-performance computing. Nature Methods, 9, 772. 10.1038/nmeth.2109Search in Google Scholar PubMed PubMed Central

Davis H.S. 1944. A revision of the genus Henneguya (Myxosporidia) with descriptions of two new species. Transactions of the American Microscopical Society, 63, 311–320. 10.2307/3223303Search in Google Scholar

Dyková I., de Buron I., Roumillat W.A., Fiala I. 2011. Henneguya cynoscioni sp. n. (Myxosporea: Bivalvulida), an agent of severe cardiac lesions in the spotted seatrout, Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitologica, 58, 169–177. 10.14411/fp.2011.017Search in Google Scholar PubMed

Edgar R.C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797. 10.1093/nar/gkh340Search in Google Scholar PubMed PubMed Central

Eiras J., Zhang J., Molnár K. 2014. Synopsis of the species of Myxobolus Bütschli, 1882 (Myxozoa: Myxosporea, Myxobolidae) described between 2005 and 2013. Systematic Parasitology, vol. 88, 11–36. 10.1007/s11230-014-9484-5Search in Google Scholar PubMed

Eiras J.C. 2002. Synopsis of the species of the genus Henneguya Thélohan, 1892 (Myxozoa: Myxosporea: Myxobolidae). Systematic Parasitology, 52, 43–54. 10.1023/A:1015016312195Search in Google Scholar

Eiras J.C., Adriano E.A. 2012. A checklist of new species of Henneguya Thélohan, 1892 (Myxozoa: Myxosporea, Myxobolidae) described between 2002 and 2012. Systematic Parasitology, 83, 95–104. 10.1007/s11230-012-9374-7Search in Google Scholar PubMed

Ferguson J.A., Atkinson S.D., Whipps C.M., Kent M.L. 2008. Molecular and morphological analysis of Myxobolus spp. of salmonid fishes with the description of a new Myxobolus species. Journal of Parasitology, 94, 1322–133410.1645/GE-1606.1Search in Google Scholar

Fiala I., Bartošová-Sojková P., Whipps C.M. 2015. Classification and Phylogenetics of Myxozoa. In: (Eds. Okamura B., Gruhl A., Bartholomew J.L.) Myxozoan Evolution, ecology and development. Springer International Publishing. pp. 85–110. 10.1007/978-3-319-14753-6Search in Google Scholar

Griffin M.J., Khoo L.H., Torrans L., Bosworth B.G., Quiniou S.M., Gaunt P.S., Pote L.M. 2009. New data on Henneguya pellis (Myxozoa: Myxobolidae), a parasite of blue catfish Ictalurus furcatus. Journal of Parasitology, 95, 1455–1467. 10.1645/GE-2106.1Search in 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. 10.1577/H07-001.1Search in Google Scholar

Gurley R.R. 1893. On the classification of the Myxosporidia, a group of protozoan parasites infesting fishes. Bulletin of the U.S. Fish Commission, 11, 407–420Search in 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. 10.3354/dao046197Search in Google Scholar

Hanson L.A., Lin D., Pote L.M.W., 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, 37–41. 10.1577/1548-8667(2001)013<0117:SSURGCO>2.0.CO;2Search in Google Scholar

Hogge C.I., Campbell M.R., Jahnson K. 2008. A new species of myxozoan (Myxosporea) from the brain and spinal cord of rainbow trout (Oncorhynchus mykiss) from Idaho. Journal of Parasitology, 94, 218–222. 10.1645/GE-1292.1Search in Google Scholar

Kent M.L., Andree K.B., Bartholomew J.L., El-Matbouli M., Desser S.S., Devlin R.H., Feist S.W., Hendrick R.P., Hoffman R.W., Khattra J., Hallet S.L., Lester R.J.G., Longshaw M., Palenzuela O., Siddall M.E., Xiao C. 2001. Recent advances in our knowledge of the Myxozoa. The Journal of Eukaryotic Microbiology, 48, 395–413. 10.1111/j.1550-7408.2001.tb00173.xSearch in Google Scholar

Khlifa S., Miller T.L., Adlard R.D., Faye N., Sasa P. 2012. Henneguya mauritaniensis n. sp. (Myxozoa) from the arterial bulb of Pagrus caeruleostictus (Valenciennes, 1830) off Mauritania. Parasitology Research, 111, 1287–1294. 10.1007/s00436-012-2963-1Search in Google Scholar

Kudo R. 1933. A Taxonomic Consideration of Myxosporidia. Transactions of the American Microscopical Society, 52, 195–216. 10.2307/3222254Search in 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. 10.1093/molbev/msw054Search in Google Scholar PubMed PubMed Central

Li Y.C., Sato H., Kamata Y., Ohnishi T., Sugita-Konishi Y. 2012. Three novel myxobolid species of genera Henneguya and Myxobolus (Myxosporea: Bivalvulida) from marine fish in Japan. Parasitology Research, 111, 819–826. 10.1007/s00436-012-2904-zSearch in Google Scholar PubMed

Lom J., Arthur J.R. 1989. A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases, 12, 151–156. 10.1111/j.1365-2761.1989.tb00287.xSearch in Google Scholar

Lom J., Dyková I. 2006. Myxozoan genera: Definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica, 53, 1–36. 10.14411/fp.2006.001Search in Google Scholar

Milanin T., Augusto A., Maia M., Ramos M., Silva M., Carriero M.M., Adriano E.A. 2015. Molecular phylogeny and ultrastructure of Myxobolus cf. cuneus, a parasite of patinga hybrid and Henneguya pseudoplatystoma, a parasite of pintado hybrid. Acta Parasitologica, 60, 442–450. 10.1515/ap-2015-0061Search in Google Scholar PubMed

Milanin T., Eiras J.C., Arana S., Maia A.A.M., Alves A.L., Silva M.R.M., Carriero M.M., Ceccarelli P.S., Adriano E.A. 2010. Phylogeny, ultrastructure, histopathology and prevalence of Myxobolus oliveirai sp. nov., a parasite of Brycon hilarii (Characidae) in the Pantanal wetland, Brazil. Memórias do Instituto Oswaldo Cruz,105, 762–769. 10.1590/S0074-02762010000600006Search in Google Scholar PubMed

Miller M.A., Pfeiffer W., Schwartz T. 2010. Creating the CIPRES Science Gateway for inference of large phylogenetic trees. In: Proceedings of the Gateway Computing Environments Workshop (GCE), 14 Nov. 2010, New Orleans, LA, pp. 1–810.1109/GCE.2010.5676129Search in Google Scholar

Minchew C.D. 1981. Unicauda magna sp. n. (Protozoa: Myxozoa): a new myxozoan from the fin tissues of the fathead minnow, Pimephales promelas Rafinesque. Journal of Fish Diseases, 4, 513–518. 10.1111/j.1365-2761.1981.tb01163.xSearch in Google Scholar

Moreira G.S.A., Adriano E.A., Silva M.R.M., Ceccarelli P.S., Maia A.A.M. 2014a. The morphological and molecular characterization of Henneguya rotunda n. sp., a parasite of the gill arch and fins of Salminus brasiliensis from the Mogi Guaçu River, Brazil. Parasitology Research, 113, 1703–1711. 10.1007/s00436-014-3815-ySearch in Google Scholar PubMed

Moreira G.S.A., Adriano E.A., Silva M.R.M., Ceccarelli P.S., Maia A.A.M. 2014b. Morphology and 18S rDNA sequencing identifies Henneguya visibilis n. sp., a parasite of Leporinus obtusidens from Mogi Guaçu River, Brazil. Parasitology Research, 113, 81–90. 10.1007/s00436-013-3629-3Search in Google Scholar PubMed

Müller M.I., Adriano E.A., Ceccarelli P.S., Da Silva M.R.M., Maia A.A.M., Ueta M.T. 2013. Prevalence, intensity, and phylogenetic analysis of Henneguya piaractus and Myxobolus cf. colossomatis from farmed Piaractus mesopotamicus in Brazil. Diseases of Aquatic Organisms,107, 129–139. 10.3354/dao02668Search in Google Scholar

Naldoni J., Maia A.A.M., Da Silva M.R.M., Adriano E.A. 2014. Henneguya cuniculator sp. nov., a parasite of spotted sorubim Pseudoplatystoma corruscans in the São Francisco Basin, Brazil. Diseases of Aquatic Organisms,107, 211–221. 10.3354/dao02685Search in Google Scholar

Naldoni J., Zatti S.A., Capodifoglio K.R.H., Milanin T., Maia A.A.M., Silva M.R.M., Adriano E.A. 2015. Host-parasite and phylogenetic relationships of Myxobolus filamentum sp. n. (Myxozoa: Myxosporea), a parasite of Brycon orthotaenia (Characiformes: Bryconidae) in Brazil. Folia Parasitologica, 62, 4–11. 10.14411/fp.2015.014Search in 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. 10.7589/0090-3558-6.4.448Search in Google Scholar

Polyanskii Y.I. 1955. The parasitology of fish of Northern marine waters of the USSR: Parasites of the fish of the Barents Sea. Trudy Zoologicheskogo Instituta Akademii Nauk USSR (Transactions of the Zoological Institute of the Academy of Sciences of the USSR), 19, 5–170 (In Russian)Search in Google Scholar

Rahemo Z.I.F. 1976. Unicauda lumae sp.n. (Myoxsporidia: Myobolidae) from a fresh water fish, Barbus grypus Heckel, from river Tigris in Iraq. Parasitenkunde, 51, 1–5. 10.1007/BF00380522Search in Google Scholar

Rambaut A. 2012. FigTree v. 1.4. Molecular evolution, phylogenetics and epidemiology. Edinburgh, UK: University of Edinburgh, Institute of Evolutionary Biology, http://tree.bio.ed.ac.uk/software/figtree/Search in Google Scholar

Ronquist F., Teslenko M., van der Mark P., Ayres D.L., Darling A., Hohna S., Larget B., Liu, L., Suchard, M.A., Huelsenbeck, J.P. 2012. MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542. 10.1093/sysbio/sys029Search in Google Scholar

Rosser T.G., Alberson N.R., Baumgartner W.A., Mauel M.J., Pote L.M., Griffin M.J. 2016. Morphological, histological and molecular description of Unicauda fimbrethilae n. sp. (Cnidaria: Myxosporea: Myxobolidae) from the intestinal tract of channel catfish Ictalurus punctatus. Journal of Parasitology, 12, 105–113. 10.1645/15-810Search in Google Scholar

Schlegel M., Lom J., Stechmann A., Bernhard D., Leipe D., Dyková I., Sogin M. 1996. Phylogenetic analysis of complete subunit ribosomal RNA coding region of Myxidium lieberkuehni: evidence that Myxozoa are Metazoa and related to the Bilateria. Archiv Für Protisten Kunde, 147, 1–9. 10.1016/S0003-9365(96)80002-9Search in Google Scholar

Shul’man S.S. 1966. Myxosporidia of the USSR. Nauka, pp. 504. (In Russian)Search in Google Scholar

Shul’man S.S. 1984. Parasitic Protozoa. In: Baeur ON, editor. Key to parasites of freshwater fishes of the USSR. Leningrad: Nauka Publishers, 1–428. (In Russian)Search in Google Scholar

Siddall M.E., Martin D.S., Bridge D., Desser S.S., Cone D.K. 1995. The demise of a Phylum of Protists: phylogeny of Myxozoa and other parasitic Cnidaria. Journal of Parasitology, 81, 961–967. 10.2307/3284049Search in Google Scholar

Smothers J., von Dohlen C., Smith L., Spall R. 1994. Molecular evidence that the myxozoan protists are metazoans. Science, 265, 1719–1721. 10.1126/science.8085160Search in Google Scholar PubMed

Vidal L.P., Luque J.L. 2017. New morphological data and molecular diagnostic of Henneguya friderici (Myxozoa: Myxobolidae), a parasite of Leporinus friderici (Osteichthyes: Anostomidae) from southeastern Brazil. Brazilian Journal of Veterinary Parasitology, 26, 81–88. 10.1590/S1984-29612017010Search in Google Scholar PubMed

Ward H.B. 1919. Notes on North American Myxosporidia. Journal of Parasitology, 6, 49–64. 10.2307/3270895Search in Google Scholar

Yokoyama H., Itoh N., Tanaka S. 2005. Henneguya pagri n. sp. (Myxozoa: Myxosporea) causing cardiac henneguyosis in red sea bream, Pagrus major (Temminck & Schlegel). Journal of Fish Diseases, 28, 479–487. 10.1111/j.1365-2761.2005.00655.xSearch in Google Scholar PubMed

Yokoyama H., Whipps C.M., Kent M.L., Mizuno K., Kawakami H. 2004. Kudoa thyrsites from Japanese flounder and Kudoa lateolabracis n. sp from chinese sea bass: Causative myxozoans of post-mortem myoliquefaction. Fish Pathology, 39, 79–85. 10.3147/jsfp.39.79Search in Google Scholar

Zatti S.A., Arana S., Maia A.A.M., Adriano E.A. 2016. Ultrastructural, ssrDNA sequencing of Myxobolus prochilodus and Myxobolus porofilus and details of the interaction with the host Prochilodus lineatus. Parasitology Research, 115, 4573–4585. 10.1007/s00436-016-5248-2Search in Google Scholar PubMed

Received: 2018-02-23
Revised: 2018-04-04
Accepted: 2018-04-10
Published Online: 2018-07-04
Published in Print: 2018-09-25

© 2018 W. Stefański Institute of Parasitology, PAS

Scroll Up Arrow