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Phylogenetic position of Sphaerospora testicularis and Latyspora scomberomori n. gen. n. sp. (Myxozoa) within the marine urinary clade

Published online by Cambridge University Press:  15 October 2010

PAVLA BARTOŠOVÁ ,
MARK A. FREEMAN ,
HIROSHI YOKOYAMA ,
MONICA CAFFARA  and
IVAN FIALA
PAVLA BARTOŠOVÁ
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
MARK A. FREEMAN
Affiliation:
Institute of Ocean and Earth Sciences, University of Malaya, Kuala Lumpur 50603, Malaysia
HIROSHI YOKOYAMA
Affiliation:
Graduate School of Agricultural and Life Sciences, The University of Tokyo, Yayoi, Bunkyo, Tokyo 113 8657, Japan
MONICA CAFFARA
Affiliation:
Department of Veterinary Public Health and Animal Pathology, University of Bologna, via Tolara di Sopra 50, 40064 Ozzano Emilia, Bologna, Italy
IVAN FIALA*
Affiliation:
Institute of Parasitology, Biology Centre, Academy of Sciences of the Czech Republic, Branišovská 31, 370 05 České Budějovice, Czech Republic Faculty of Science, University of South Bohemia, Branišovská 31, 370 05 České Budějovice, Czech Republic
*
*Corresponding author: Institute of Parasitology, Biology Centre ASCR, Branišovská 31, 370 05 České Budějovice, Czech Republic. Tel: +420 38 7775425. Fax: +420 38 5310388. E-mail: [email protected]
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Summary

An amendment of the family Sinuolineidae (Myxosporea) is proposed in order to include a newly described genus Latyspora n. gen. The type species Latyspora scomberomori n. gen. n. sp. is a coelozoic parasite in the kidney tubules of Scomberomorus guttatus. In addition to the morphological and molecular characterization of L. scomberomori n. gen. n. sp., we also present novel SSU rDNA data on Sphaerospora testicularis, a serious parasite of Dicentrarchus labrax. Performed phylogenetic analyses revealed that both species cluster within the marine urinary clade encompassing the representatives with a shared insertion within their V4 SSU rRNA region and grouping according to the shape of their spores’ sutural line and their similar tissue tropism in the host. Sphaerospora testicularis is the closest relative to Parvicapsula minibicornis within the Parvicapsula subclade and L. scomberomori n. gen. n. sp. is the basal species of the Zschokkella subclade. The phylogenetic position of S. testicularis, outwith the basal Sphaerospora sensu stricto clade, and its morphology suggest it being a non-typical Sphaerospora. The sequence data provided on S. testicularis can help in future revisions of the strongly polyphyletic genus Sphaerospora. We recommend re-sequencing of several sphaerosporids as an essential step before such taxonomic changes are accomplished.

Keywords

MyxosporeaSphaerosporaLatysporaScomberomorusDicentrarchusSSU rDNAsutural linemarine urinary clade
Type
Research Article
Information
Parasitology , Volume 138 , Issue 3 , March 2011 , pp. 381 - 393
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Adlard, R. D., Bryant, M. S., Whipps, C. M. and Kent, M. L. (2005). Multivalvulid myxozoans from eastern Australia: Three new species of Kudoa from scombrid and labrid fishes of the Great Barrier Reef, Queensland, Australia. Journal of Parasitology 91, 1138–1142.CrossRefGoogle ScholarPubMed
Auerbach, M. (1909). Biologische und morphologische Bemerkungen über Myxosporidien. Zoologischer Anzeiger 35, 57–63.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, 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, 262–271.Google Scholar
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 an effective tool for their molecular phylogenetics. Molecular Phylogenetics and Evolution 53, 81–93. doi: 10.1016/j.ympev.2009.05.018.CrossRefGoogle ScholarPubMed
Baska, F. (1987). Histological studies on the development of Myxobolus pseudodispar Gorbunova, 1936 in the roach (Rutilus rutilus). Acta Veterinaria Hungarica 35, 251–257.Google ScholarPubMed
Cho, J. B. and Kim, K. H. (2001). Light and electron microscopic observations of Leptotheca koreana n. sp. (Myxosporea) in the kidney of cultured rockfish Sebastes schlegeli. Diseases of Aquatic Organisms 46, 189–195.Google Scholar
Davis, H. S. (1917). Myxosporidia of the Beaufort region, a systematic and biological study. Washington Bulletin of Unites States Bureau of Fishery 35, 203–243.Google Scholar
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, 1434–1442.Google Scholar
Diamant, A., Ucko, M., Paperna, I., Colorni, A. and Lipshitz, A. (2005). Kudoa iwatai (Myxosporea: Multivalvulida) in the wild and cultured fish in the Red Sea: redescription and molecular phylogeny. Journal of Parasitology 91, 1175–1189.Google Scholar
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, 469–478.CrossRefGoogle ScholarPubMed
Feist, S. W., Chilmonczyk, S. and Pike, A. W. (1991). Structure and development of Sphaerospora elegans Thélohan, 1892 (Myxozoa: Myxosporea) in the sticklebacks Gasterosteus aculeatus L. and Pungitius pungitius L. (Gasterosteidae). European Journal of Protistology 27, 269–277.Google Scholar
Fiala, I. (2006). The phylogeny of Myxosporea (Myxozoa) based on small subunit ribosomal RNA gene analysis. International Journal for Parasitology 36, 1521–1534. doi: 10.1016/j.ijpara.2006.06.016.Google Scholar
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. doi:10.1186/1471-2148-10-228.Google Scholar
Fioravanti, M. L., Caffara, M., Florio, D., Gustinelli, A. and Marcer, F. (2004). Sphaerospora dicentrarchi and S. testicularis (Myxozoa: Sphaerosporidae) in farmed European sea bass (Dicentrarchus labrax) from Italy. Folia Parasitologica 51, 208–210.Google Scholar
Fioravanti, M. L., Caffara, M., Florio, D., Gustinelli, A. and Marcer, F. (2006). A parasitological survey of European sea bass (Dicentrarchus labrax) and gilthead sea bream (Sparus aurata) cultured in Italy. Veterinary Research Communications 30, 249–252. doi: 10.1007/s11259-006-0053-5.Google Scholar
Freeman, M. A., Yokoyama, H. and Ogawa, K. (2008). Description and phylogeny of Ceratomyxa anko sp. n. and Zschokkella lophii sp. n. from the Japanese anglerfish, Lophius litulon (Jordan). Journal of Fish Diseases 31, 921–930. doi: 10.1111/j.1365-2761.2008.00965.x.Google Scholar
Gunter, N. and Adlard, R. (2010). The demise of Leptotheca Thélohan, 1895 (Myxozoa: Myxosporea: Ceratomyxidae) and assignment of its species to Ceratomyxa Thélohan, 1892 (Myxosporea: Ceratomyxidae), Ellipsomyxa Køie, 2003 (Myxosporea: Ceratomyxidae), Myxobolus Bütschli, 1882 and Sphaerospora Thélohan, 1892 (Myxosporea: Sphaerosporidae). Systematic Parasitology 75, 81–104. doi: 10.1007/s11230-009-9227-1.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, 95–98.Google Scholar
Hallett, S. L. and 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.Google Scholar
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, 1099–1111. doi: 10.1016/j.ijpara.2004.06.002.Google Scholar
Holzer, A. S., Wooten, 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, 1281–1295. doi: 10.1016/j.ijpara.2007.03.014.Google Scholar
Holzer, A. S., Wootten, R. and Sommerville, C. (2010). Zschokkella hildae Auerbach, 1910: phylogenetic position, morphology, and location in cultured Atlantic cod. Parasitology International 59, 133–140.Google Scholar
Jirků, M., Fiala, I. and Modrý, 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, 1727–1739. doi: 10.1017/S0031182007003241.Google Scholar
Jones, S., Prosperi-Porta, G. and Dawe, S. (2006). A new parvicapsulid (Myxosporea) species in adult pink salmon, Oncorhynchus gorbuscha, from the Quinsam River, British Columbia, Canada. Journal of Parasitology 92, 1313–1318.Google Scholar
Kardong, K. (2008). Vertebrates: Comparative Anatomy, Function, Evolution, 5th Edn. McGraw-Hill, Boston, MA, USA.Google Scholar
Kent, M. L., Andree, K. B., Bartholomew, J. L., El-Matbouli, M., Desser, S. S., Devlin, R. H., Feist, S. W., Hedrick, R. P., Hoffmann, R. W., Khattra, J., Hallett, S. L., Lester, R. J. G., Longshaw, M., Palenzuela, O., Siddall, M. E. and Xiao, C. (2001). Recent advances in our knowledge of the Myxozoa. Journal of Eukaryotic Microbiology 48, 395–413.Google Scholar
Køie, M., Karlsbakk, E. and Nylund, A. (2007). A new genus Gadimyxa with three new species (Myxozoa, Parvicapsulidae) parasitic in marine fish (Gadidae) and the two-host life cycle of Gadimyxa atlantica n. sp. Journal of Parasitology 93, 1459–1467.Google Scholar
Kpatcha, T. K., Diebakate, C. and Toguebaye, B. S. (1996). Myxosporidies (Myxozoa, Myxosporea) des genres Sphaeromyxa Thélohan, 1892, Myxidium Bütschli, 1882, Zschokkella Auerbach, 1910, Bipteria Kovaljova, Zubtchenko & Krasin, 1983 et Leptotheca Thélohan, 1895 parasites des poisons des côtes sénégalaises (Afrique de l'Ouest). Journal of African Zoology 110, 309–317.Google Scholar
Lom, J. and Arthur, J. R. (1989). A guideline for the preparation of species descriptions in Myxosporea. Journal of Fish Diseases 12, 151–156.CrossRefGoogle Scholar
Maddison, W. P. and Maddison, D. R. (2009). Mesquite: a modular system for evolutionary analysis. Version 2.72. www.mesquiteproject.orgGoogle Scholar
Morris, D. J. and Adams, A. (2008). Sporogony of Tetracapsuloides bryosalmonae in the brown trout Salmo trutta and the role of the tertiary cell during the vertebrate phase of myxozoan life cycles. Parasitology 135, 1075–1092. doi: 10.1017/S0031182008004605.Google Scholar
Nylund, A., Karlsbakk, E., Sæther, P. A., Koren, C., Larsen, T., Nielsen, B. D., Broderud, A. E., Hostlund, C., Fjellsoy, K. R., Lervik, K. and Rosnes, L. (2005). Parvicapsula pseudobranchicola (Myxosporea) in farmed Atlantic salmon Salmo salar: tissue distribution, diagnosis and phylogeny. Diseases of Aquatic Organisms 63, 197–204.Google Scholar
Posada, D. (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256. doi: 10.1093/molbev/msn083.Google Scholar
Ronquist, F. and Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574. doi: 10.1093/bioinformatics/btg180.Google Scholar
Schluter, D., Price, T., Mooers, A. O. and Ludwig, D. (1997). Likelihood of ancestor states in adaptive radiation. Evolution 51, 1699–1711.Google Scholar
Sitjà-Bobadilla, A. (2009). Can Myxosporean parasites compromise fish and amphibian reproduction? Proceedings of the Royal Society of London, B 276, 2861–2870. doi: 10.1098/rspb.2009.0368.Google Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (1990). Sphaerospora testicularis sp. nov. (Myxosporea: Sphaerosporidae) in wild and cultured sea bass, Dicentrarchus labrax (L.), from the Spanish Mediterranean area. Journal of Fish Diseases 13, 193–203.Google Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (1992). Light and electron-microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea, Sphaerosporidae) from wild and cultured sea bass, Dicentrachus labrax L. Journal of Protozoology 39, 273–281.Google Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (1993). Ultrastructural and cytochemical observations on the sporogenesis of Sphaerospora testicularis (Protozoa, Myxosporea) from Mediterranean sea bass, Dicentrarchus labrax (L.). European Journal of Protistology 29, 219–229.Google Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (1995). Light and electron-microscopic description of Polysporoplasma n. g. (Myxosporea, Bivalvulida), Polysporoplasma sparis n. sp. from Sparus aurata (L.) and Polysporoplasma mugilis n. sp. from Liza aurata L. European Journal of Protistology 31, 77–89.Google Scholar
Sitjà-Bobadilla, A. and Alvarez-Pellitero, P. (2001). Leptotheca sparidarum n. sp. (Myxosporea: Bivalvulida), a parasite from cultured common dentex (Dentex dentex L.) and gilthead sea bream (Sparus aurata L.) (Teleostei: Sparidae). Journal of Eukaryotic Microbiology 48, 627–639.CrossRefGoogle Scholar
Swofford, D. L. (2001). PAUP*. Phylogenetic Analysis Using Parsimony (* and Other Methods). Version 4. Sinauer Associates, Sunderland, Massachusetts, USA.Google Scholar
Thélohan, P. (1895). Recherches sur les Myxosporidies. Bulletin Scientifique de France et Belgie 26, 100–394.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and Higgins, D. G. (1997). The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 24, 4876–4882.Google Scholar
Tun, T., Yokoyama, H., Ogawa, K. and Wakabayashi, H. (2000). Myxosporeans and their hyperparasitic microsporeans in the intestine of emaciated tiger puffer. Fish Pathology 35, 145–156.Google Scholar
Whipps, C. M., Adlard, R. D., Bryant, M. S. and Kent, M. L. (2003). Two unusual myxozoans, Kudoa quadricornis n. sp (Multivalvulida) from the muscle of goldspotted trevally (Carangoides fulvoguttatus) and Kudoa permulticapsula n. sp (Multivalvulida) from the muscle of spanish mackerel (Scomberomorus commerson) from the Great Barrier Reef, Australia. Journal of Parasitology 89, 168–173.CrossRefGoogle Scholar