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‘Who's who’ in renal sphaerosporids (Bivalvulida: Myxozoa) from common carp, Prussian carp and goldfish – molecular identification of cryptic species, blood stages and new members of Sphaerospora sensu stricto

  • ASTRID SIBYLLE HOLZER (a1), P. BARTOŠOVÁ (a1), H. PECKOVÁ (a1), T. TYML (a1) (a2), S. ATKINSON (a3), J. BARTHOLOMEW (a3), D. SIPOS (a4), E. ESZTERBAUER (a4) and I. DYKOVÁ (a1) (a5)...
Summary

Myxozoans are a group of diverse, spore-forming metazoan microparasites bound to aquatic environments. Sphaerospora dykovae (previously S. renicola) causes renal sphaerosporosis and acute swim bladder inflammation (SBI) in juvenile Cyprinus carpio carpio, in central Europe. A morphologically similar species with comparably low pathogenicity, S. angulata has been described from C. c. carpio, Carassius auratus auratus and Carassius gibelio. To clarify uncertainties and ambiguities in taxon identification in these hosts we decided to re-investigate differences in spore morphology using a statistical approach, in combination with SSU and LSU rDNA sequence analyses. We found that developing spores of S. angulata and S. dykovae cannot be distinguished morphologically and designed a duplex PCR assay for the cryptic species that demonstrated S. dykovae is specific to C. c. carpio, whereas S. angulata infects C. a. auratus and C. gibelio. The molecular identification of myxozoan blood stages in common carp and goldfish, which had previously been ascribed to Sphaerospora spp. showed that approximately 75% of blood stages were from non-sphaerosporid coelozoic species infecting these cyprinids and more than 10% were from an alien species, Myxobilatus gasterostei, developing in sticklebacks. We hereby report non-selective myxozoan host invasion and multi-species infections, whose role in SBI still requires clarification.

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Corresponding author
*Corresponding author: Institute of Parasitology, Biology Centre of the Academy of Sciences of the Czech Republic, Branišovská 31, 37005 České Budějovice, Czech Republic. Tel: +420 38777 5424. Fax: +420 38 5310388. E-mail: astrid.holzer@paru.cas.cz
References
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Alama-Bermejo, G., Raga, J. and Holzer, A. S. (2011). Host-parasite relationship of Ceratomyxa puntazzi n. sp (Myxozoa: Myxosporea) and sharpsnout seabream Diplodus puntazzo (Walbaum, 1792) from the Mediterranean with first data on ceratomyxid host specificity in sparids. Veterinary Parasitology 182, 181192.
Arthur, R. and Lom, J. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151156.
Asahida, T., Kobayashi, T., Saitoh, K. and Nakayama, I. (1996). Tissue preservation and total DNA extraction from fish stored at ambient temperature using buffers containing high concentration of urea. Fisheries Science 62, 727730.
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.
Bartošová, P., Fiala, I. and Hypša, V. (2009). Concatenated SSU and LSU rDNA data confirm the main evolutionary trends within myxosporeans (Myxozoa: Myxosporea) and provide effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution 53, 8193.
Bartošová, P. and Fiala, I. (2011). Molecular evidence for the existence of cryptic species assemblages of several myxosporeans (Myxozoa). Parasitology Research 108, 573583.
Bartošová, P., Fiala, I., Cinková, M., Sipos, E., Eszterbauer, E., Jirku, M., Caffara, M., Fioravanti, M. L. and lzer, A. S. (2011 b). Sphaerospora sensu stricto clade (Myxozoa): Taxonomy and phylogeny obased on the ribosomal and protein-coding data. Abstract Book, International Conference on Dieseases of Fish and Shellfish, Split, September 12–16, 2011, 62.
Bartošová, P., Freeman, M. A., Yokoyama, H., Caffara, M. and Fiala, I. (2011 a). Phylogenetic position of Sphaerospora testicularis and Latyspora scomberomori n. gen. n. sp (Myxozoa) within the marine urinary clade. Parasitology 138, 381393.
Baska, F. and Molnár, K. (1988). Blood stages of Sphaerospora spp. (Myxosporea) in cyprinid fishes. Diseases of Aquatic Organisms 5, 2328.
Björk, S. J. and Bartholomew, J. L. (2010). Invasion of Ceratomyxa shasta (Myxozoa) and comparison of migration to the intestine between susceptible and resistant fish hosts. International Journal for Parasitology 40, 10871095.
Csaba, G. (1976). An unidentifiable extracellular sporozoan parasite from the blood of the carp. Parasitologia Hungarica 9, 2124.
Csaba, G., Kovács-Gayer, E., Bekesi, L., Bucsek, M. and Szakolczai, J. (1984). Studies into the possible protozoan aetiology of swimbladder inflamation in carp fry. Journal of Fish Diseases 7, 3956.
Diamant, A., Whipps, C. M. and Kent, M. L. (2004). A new species of Sphaeromyxa (Myxosporea : Sphaeromyxina : Sphaeromyxidae) in devil firefish, Pterois miles (Scorpaenidae), from the northern Red Sea: Morphology, ultrastructure, and phylogeny. Journal of Parasitology 90, 14341442.
Drummond, A. J. and Rambaut, A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evolutionary Biology 7, 214.
Dyková, I. and Lom, J. (1988). Review of pathogenic myxosporeans in intensive culture of carp (Cyprinus carpio) in Europe. Folia Parasitologica 35, 289307.
Dyková, I., Lom, J. and Cirkovic, M. (1986). Brain myxoboliasis of the common carp (Cyprinus carpio) due to Myxobolus encephalicus. Bulletin of the European Association of Fish Pathologists 6, 1012.
El-Matbouli, M., Hoffmann, R. W. and Mandok, C. (1995). Light and electron-microscopic observations on the route of the Triactinomyxon sporoplasm of Myxobolus cerebralis from epidermis into rainbow trout cartilage. Journal of Fish Biology 46, 919935.
Eszterbauer, E. (2011). Molecular phylogeny of the kidney-parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp. from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica 59, 409409.
Eszterbauer, E., Marton, S., Rácz, O. Z., Letenyei, M. and Molnár, K. (2006). Morphological and genetic differences among actinosporean stages of fish-parasitic myxosporeans (Myxozoa): difficulties of species identification. Systematic Parasitology 65, 97114.
Eszterbauer, E. and Székely, C. (2004). Molecular phylogeny of the kidney-parasitic Sphaerospora renicola from common carp (Cyprinus carpio) and Sphaerospora sp from goldfish (Carassius auratus auratus). Acta Veterinaria Hungarica 52, 469478.
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 15211534.
Fiala, I. and Bartošová, P. (2010). History of myxozoan character evolution on the basis of rDNA and EF-2 data. BMC Evolutionary Biology 10, 228.
Fiala, I. and Dyková, I. (2004). The phylogeny of marine and freshwater species of the genus Chloromyxum Mingazzini, 1890 (Myxosporea : Bivalvulida) based on small subunit ribosomal RNA gene sequences. Folia Parasitologica 51, 211214.
Fujita, T. (1912). Notes on new sporozoan parasites of fishes. Zoologischer Anzeiger 37, 251261.
George-Nascimento, M., Lobos, V., Torrijos, C. and Khan, R. (2004). Species composition of assemblages of Ceratomyxa (Myxozoa), parasites of lings Genypterus (Ophidiidae) in the southeastern Pacific Ocean: An ecomorphometric approach. Journal of Parasitology 90, 13521355.
Grabner, D. S. and El-Matbouli, M. (2010). Experimental transmission of malacosporean parasites from bryozoans to common carp (Cyprinus carpio) and minnow (Phoxinus phoxinus). Parasitology 137, 629639.
Grupcheva, G., Dyková, I. and Lom, J. (1985). Seasonal fluctuation in the prevalence of Sphaerospora renicola and myxosporean blood-stream stages in carp fingerlings in Bulgaria. Folia Parasitologica 32, 193203.
Gunter, N. L., Whipps, C. M. and Adlard, R. D. (2009). Ceratomyxa (Myxozoa: Bivalvulida): Robust taxon or genus of convenience? International Journal for Parasitology 39, 13951405.
Gunter, N. L. and Adlard, R. D. (2010). The demise of Leptotheca Thelohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thelohan, 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Koie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Butschli, 1882 and Sphaerospora Thelohan, 1892 (Myxosporea: Sphaerosporidae). Systematic Parasitology 75, 81104.
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.
Hallett, S. L., Atkinson, S. D. and El-Matbouli, M. (2002). Molecular characterisation of two aurantiactinomyxon (Myxozoa) phenotypes reveals one genotype. Journal of Fish Diseases 25, 627631.
Hallett, S. L. and Bartholomew, J. L. (2006). Application of a real-time PCR assay to detect and quantify the myxozoan parasite Ceratomyxa shasta in river water samples. Diseases of Aquatic Organisms 71, 109118.
Holzer, A. S., Sommerville, C. and Wootten, R. (2003). Tracing the route of Sphaerospora truttae from the entry locus to the target organ of the host, Salmo salar L., using an optimized and specific in situ hybridization technique. Journal of Fish Diseases 26, 647655.
Holzer, A. S., Sommerville, C. and Wootten, R. (2004). Molecular relationships and phylogeny in a community of myxosporeans and actinosporeans based on their 18S rDNA sequences. International Journal for Parasitology 34, 10991111.
Holzer, A. S., Sommerville, C. and Wootten, R. (2006). Molecular studies on the seasonal occurrence and development of five myxozoans in farmed Salmo trutta L. Parasitology 132, 193205.
Holzer, A. S., Wootten, R. and Sommerville, C. (2007). The secondary structure of the unusually long 18S ribosomal RNA of the myxozoan Sphaerospora truttae and structural evolutionary trends in the Myxozoa. International Journal for Parasitology 37, 12811295.
Jirků, M., Fiala, I. and Modry, D. (2007). Tracing the genus Sphaerospora: rediscovery, redescription and phylogeny of the Sphaerospora ranae (Morelle, 1929) n. comb. (Myxosporea, Sphaerosporidae), with emendation of the genus Sphaerospora. Parasitology 134, 17271739.
Kallert, D. M., Bauer, W., Haas, W. and El-Matbouli, M. (2011). No shot in the dark: Myxozoans chemically detect fresh fish. International Journal for Parasitology 41, 271276.
Kallert, D. M., Eszterbauer, E., Grabner, D. and El-Matbouli, M. (2009). In vivo exposure of susceptible and non-susceptible fish species to Myxobolus cerebralis actinospores reveals non-specific invasion behaviour. Diseases of Aquatic Organisms 84, 123130.
Kent, M. L. and Lom, J. (1986). Development of the PKX myxosporean in rainbow trout Salmo gairdneri. Diseases of Aquatic Organisms 1, 159182.
Kolářová, L. (2007). Schistosomes causing cercarial dermatitis: a mini-review of current trends in systematics and a host specificity and pathogenicity. Folia Parasitologica 54, 8187.
Kovács-Gayer, E., Csaba, G., Bekesi, L., Bucsek, M., Szakolczai, J. and Molnár, K. (1982). Studies on the protozoan etiology of swim bladder inflammation in common carp fry. Bulletin of the European Association of Fish Pathologists 2, 2224.
Kovács-Gayer, E. (1983). Histopathological studies on protozoan swimbladder inflammation of common carp fry. Parasitologia Hungarica 16, 3946.
Körting, W. (1982). Protozoan parasites associated with swim-bladder inflammation (SBI) in young carp. Bulletin of the European Association of Fish Pathologists 2, 2528.
Körting, W. and Hermanns, W. (1984). Myxosporidien-Infektionen in der Niere des Karpfens (Cyprinus carpio L.) aus niedersächsischen Teichwirtschaften. Berliner und Münchner Tierärztliche Wochenschrift 97, 255259.
Körting, W., Kruse, P. and Steinhaben, D. (1989). Developmento of “Csaba cells” in experimentally infected Cyprinus carpio. Angewandte Parasitologie 30, 185188.
Lom, J. and Dyková, I. (1982). Sphaerospora renicola n. sp., a myxosporean from carp kidney, and its pathogenicity. Zeitschrift für Parasitenkunde 68, 259268.
Lom, J., Pavlásková, M. and Dyková, I. (1985). Notes on kidney-infecting species on the genus Sphaerospora Thélohan (Myxosporea), including a new species S. gobionis sp. nov., and on myxosporean life cycle stage in the blood of some freshwater fish. Journal of Fish Diseases 8, 221232.
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 136.
Lom, J., Dyková, I. and Pavlásková, M. (1983). Unidentified mobile protozoans from the blood of carp and some unsolved problems of myxosporean life cycles. Journal of Protozoology 30, 497598.
Lusková, V., Lusk, S., Halačka, K. and Vetešník, L. (2010). Carassius auratus gibelio—the most successful invasive fish in waters of the Czech Republic. Russian Journal of Biological Invasions 1, 176180.
Martinsen, E., Waite, J. and Schall, J. (2007). Morphologically defined subgenera of Plasmodium from avian hosts: test of monophyly by phylogenetic analysis of two mitochondrial genes. Parasitology 134, 483490.
May, R. M. and Nowak, M. A. (1955). Coinfection and the evolution of parasite virulence. Proceedings of the Royal Society of London, B 261, 209215.
McGeorge, J., Sommerville, C. and Wootten, R. (1996). Epizootiology of Sphaerospora truttae (Myxozoa: Myxosporea) infections in Atlantic salmon Salmo salar at freshwater smolt producing hatcheries in Scotland. Diseases of Aquatic Organisms 26, 3341.
Molnár, K. (1980 a). Renal sphaerosporosis in the common carp Cyprinus carpio L. Journal of Fish Diseases 3, 1119.
Molnár, K. (1980 b). “Sphaerosporosis”, a new kidney disease of the common carp. Fish diseases. Third COPRAQ Cooperative Programme of Research on Aquaculture Session, Munich, Federal Republic of Germany, 23–26 October 1979. Proceedings, pp. 157164.
Molnár, K. (1994). Comments on the host, organ and tissue specificity of fish myxosporeans and on the types of their intrapiscine development. Parasitologia Hungarica 27, 520.
Molnár, K., El Mansy, A., Szekely, C. and Baska, F. (1999). Experimental identification of the actinosporean stage of Sphaerospora renicola Dykova & Lom 1982 (Myxosporea : Sphaerosporidae) in oligochaete alternate hosts. Journal of Fish Diseases 22, 143153.
Molnár, K. and Kovács-Gayer, E. (1986). Experimental induction of Sphaerospora renicola (Myxosporea) infection in the common carp (Cyprinus carpio) by transmission of SB-protozoans. Zeitschrift fuer Angewandte Ichthyologie 2, 8694.
Molnár, K., Marton, S., Székely, C. and Eszterbauer, E. (2010). Differentiation of Myxobolus spp. (Myxozoa: Myxobolidae) infecting roach (Rutilus rutilus) in Hungary. Parasitology Research 107, 11371150.
Odening, K. (1987). Sphaerospora renicola (Myxosporidia), der Erreger der protozoären Schwimmblasentzündung des Jungkarpfens (renicola-Sphaerosporose). Merkblätter über angewandte Parasitenkunde und Schädlingsbekämpfung 30, 116.
Özer, A. and Wootten, R. (2000). The life cycle of Sphaerospora truttae (Myxozoa : Myxosporea) and some features of the biology of both the actinosporean and myxosporean stages. Diseases of Aquatic Organisms 40, 3339.
Özer, A., Wootten, R. and Shinn, A. P. (2002). Infection prevalence, seasonality and host specificity of actinosporean types (Myxozoa) in an Atlantic salmon fish farm located in Northern Scotland. Folia Parasitologica 49, 263268.
Papoušek, I. (2008). Molecular-genetic analysis of the species of the genus Carassius in Central Europe. Ph. D. thesis, Masaryk University of Brno, Czech Republic. http://is.muni.cz/th/21842/prif_d/Disertace_Papousek_I_cast.pdf
Price, T., Lovette, I. J., Bermingham, E., Gibbs, H. L. and Richman, A. D. (2000). The imprint of history on communities of North American and Asian warblers. American Naturalist 156, 354367.
Read, A. F. and Taylor, L. H. (2001). The ecology of genetically diverse infections. Science 292, 10991102.
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 15721574.
Sedlaczek, J., Friede, H., Kluss, P. and Vinzelberg, R. (1990). Zum jahreszeitlichen Auftreten der Schwimmblasenentzündung im Verlauf der renicola-Sphaerosporose bei Karpfen. Angewandte Parasitologie 31, 219229.
Shulman, S. S. (1966). Myxosporidia of the USSR, 1st Edn. Nauka Publishers, Moskva-Leningrad, USSR.
Singh, B. and Simon Divis, P. C. (2009). Orangutans not infected with Plasmodium vivax or P. cynomolgi, Indonesia. Emerging Infectious Diseases 15, 16571658.
Sitja-Bobadilla, A. (2008). Fish immune response to myxozoan parasites. Parasite-Journal de la Societe Francaise de Parasitologie 15, 420425.
Sitja-Bobadilla, A. and Alvarez-Pellitero, P. (1994). Revised classification and key species of the genus Sphaerospora Davies, 1917 (Protozoa: Myxosporea). Research and Reviews in Parasitology 54, 6780.
Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22, 26882690.
Swofford, D. L. (2001). PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland, MA, USA.
Ter Höfte, B. B., Körting, W. and Lehmann, J. (1984). “C- und K-Protozoen”, Endoparasiten unsicherer systematischer Zuordnung beim jungen Karpfen (Cyprinus carpio L.). Derzeitiger Wissensstand und bildliche Dokumentation. Fisch und Umwelt 13, 8999.
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 48764882.
Valkiūnas, G., Santiago-Alarcon, D., Levin, I. I., Iezhova, T. A. and Parker, P. G. (2010). A new Haemoproteus species (Haemosporida: Haemoproteidae) from the endemic galapagos dove Zenaida galapagoensis, with remarks on the parasite distribution, vectors, and molecular diagnostics. Journal of Parasitology 96, 783792.
Van Buskirk, J. (2002). A comparative test of the adaptive plasticity hypothesis: Relationships between habitat and phenotype in anuran larvae. American Naturalist 160, 87102.
Van der Auwera, G., Chapelle, S. and Dewachter, R. (1994). Structure of the large ribosomal subunit RNA of Phytophthora megasperma, and phylogeny of the oomycetes. FEBS Letters 338, 133136.
Xiao, C. X. and Desser, S. S. (1998). The oligochaetes and their actinosporean parasites in Lake Sasajewun, Algonquin Park, Ontario. Journal of Parasitology 84, 10201026.
Yokoyama, H. (1997). Transmission of Thelohanellus hovorkai Achmerov, 1960 (Myxosporea: Myxozoa) to common carp Cyprinus carpio through the alternate oligochaete host. Systematic Parasitology 36, 7984.
Yokoyama, H., Ogawa, K. and Wakabayashi, H. (1995). Chemoresponse of actinosporean spores of Myxobolus cultus to skin mucus of goldfish Carassius auratus. Diseases of Aquatic Organisms 21, 711.
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