Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-02T21:28:07.620Z Has data issue: false hasContentIssue false

Ultrastructural and molecular studies of Microgemma carolinus n. sp. (Microsporidia), a parasite of the fish Trachinotus carolinus (Carangidae) in Southern Brazil

Published online by Cambridge University Press:  19 July 2012

G. CASAL
Affiliation:
Laboratory of Pathology, Interdisciplinary Centre of Marine and Environmental Research, University of Porto (CIIMAR-UP), Rua dos Bragas, 177, 4050-123 Porto, Portugal Departmento de Ciências, Instituto Superior de Ciências da Saúde – Norte, CESPU, 4585-116 Gandra, Portugal Department of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP), University of Porto, 4050-313 Porto, Portugal
E. MATOS
Affiliation:
Carlos Azevedo Research Laboratory, Federal Rural University of Amazonia, 66077-530 Belém, PA, Brazil
P. GARCIA
Affiliation:
Laboratory of Diagnostic and Pathology in Aquaculture, Federal University of Santa Catarina, 88040-970 Florianópolis, SC, Brazil
S. AL-QURAISHY
Affiliation:
Zoology Department, College of Science, King Saud University, 11451 Riyadh, Saudi Arabia
C. AZEVEDO*
Affiliation:
Laboratory of Pathology, Interdisciplinary Centre of Marine and Environmental Research, University of Porto (CIIMAR-UP), Rua dos Bragas, 177, 4050-123 Porto, Portugal Department of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP), University of Porto, 4050-313 Porto, Portugal
*
*Corresponding author: Department of Cell Biology, Institute of Biomedical Sciences (ICBAS/UP), University of Porto, Rua de Jorge Viterbo Ferreira, no. 228, 4050-313 Porto, Portugal. Tel: +351 220 428 241. E-mail: [email protected]

Summary

A new species of Microsporidia Microgemma carolinus n. sp. found in the marine teleost Trachinotus carolinus collected in Florianópolis, Brazil was described based on light, ultrastructural and phylogenetic studies. This parasite developed in the liver forming whitish xenomas that contained different developmental stages with monokaryotic nuclei. The periphery of the xenoma presented some vacuolization and possessed several small projections in the membrane. The mature spores, measuring 3·8 ± 0·4 μm in length and 2·4 ± 0·4 μm in width, were slightly pyriform to ellipsoidal and had rounded ends. The polaroplast was bipartite and the isofilar polar filament was coiled with 8 – 9 turns in a single or double row at the posterior end of the spore. The nucleus was voluminous and in a central position, measuring ∼0·9 μm in diameter. A large posterior vacuole appeared as a pale area, occupying about a third of the spore length. The SSU rRNA gene was sequenced and analysed using maximum parsimony, maximum likelihood and neighbour-joining methods. This study allowed us to conclude that this was a new species of the genus Microgemma, being the first description of this genus from among South America fauna.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Amigó, J. M., Salvadó, H., Gracia, M. P. and Vivarès, C. P. (1996). Ultrastructure and development of Microsporidium ovoideum (Thélohan, 1895) Sprague, 1977, a microsporidian parasite of the red band fish (Cepola macrophthalma L.). European Journal of Protistology 32, 532538.CrossRefGoogle Scholar
Amigó, J. M., Salvadó, H. and Gracia, M. L. (1998). The pathologic cycle of the infection of the microsporidian Microgemma ovoidea (Thèl., 1895) Amigó et al. 1996 in the liver of the Red band fish (Cepola macrophthalma L.) Parasitology Research 84, 712.Google ScholarPubMed
Azevedo, C. and Matos, E. (2002). Fine structure of a new species, Loma myrophis (Phylum Microsporidia), parasite of the Amazonian fish Myrophis platyrhynchus (Teleostei, Ophichthidae). European Journal of Protistology 37, 445452.CrossRefGoogle Scholar
Azevedo, C. and Matos, E. (2003). Amazonspora hassar n. gen. and n. sp. (phylum Microsporidia, fam. Glugeidae), a parasite of the Amazonian teleost Hassar orestis (fam. Doradidae). Journal of Parasitology 89, 336341.CrossRefGoogle Scholar
Baquero, E., Rubio, M., Moura, I. N. S., Pieniazek, N. Y. and Jordana, R. (2005). Myosporidium merluccius n. g., n. sp. infecting muscle of commercial hake (Merluccius sp.) from fisheries near Namibia. The Journal of Eukaryotic Microbiology 52, 476483.CrossRefGoogle Scholar
Canning, E. U. and Curry, A. (2005). Microgemma vivaresi (Microsporidia: Tetramicridae): host reaction to xenomas induced in sea scorpions, Taurulus bubalis (Osteichthyes: Cottidae). Folia Parasitologica 52, 95102.CrossRefGoogle ScholarPubMed
Canning, E. U., Feist, S. W., Longshaw, M., Okamura, B., Anderson, C. L., Tse, M. T. and Curry, A. (2005). Microgemma vivaresi n. sp. (Microsporidia, Tetramicridae), infecting liver and skeletal muscle of sea scorpions, Taurulus bubalis (Euphrasen, 1786) (Osteichthyes, Cottidae), an inshore, littoral fish. The Journal of Eukaryotic Microbiology 52, 123131.CrossRefGoogle Scholar
Canning, E. U. and Lom, J. (1986). The Microsporidia of Vertebrates. Academic Press, London, UK.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.CrossRefGoogle Scholar
Casal, G., Matos, E., Teles-Grilo, M. L. and Azevedo, C. (2008). A new microsporidian parasite, Potaspora morhaphis n. gen., n. sp. (Microsporidia) infecting the Teleostean fish, Potamorhaphis guianensis from the River Amazon. Morphological, ultrastructural and molecular characterization. Parasitology 135, 10531064.CrossRefGoogle Scholar
Casal, G., Matos, E., Teles-Grilo, M. L. and Azevedo, C. (2009). Morphological and genetical description of Loma psittaca sp. n. isolated from the Amazonian fish species Colomesus psittacus. Parasitology Research 105, 12611271.CrossRefGoogle Scholar
Casal, G., Matos, E., Teles-Grilo, L. and Azevedo, C. (2010). Ultrastructural and molecular characterization of a new microsporidium parasite from the Amazonian fish, Gymnorhamphichthys rondoni (Rhamphichthyidae). Journal of Parasitology 96, 11551163.CrossRefGoogle ScholarPubMed
Cellere, E. F., Cordeiro, N. S. and Adriano, E. A. (2002). Myxobolus absonus sp. n. (Myxozoa: Myxosporea) parasitizing Pimelodus maculatus (Siluriformes: Pimelodidae), a South American freshwater fish. Memorias do Instituto Oswaldo Cruz 97, 7980.CrossRefGoogle Scholar
Cheney, S. A., Lafranchi-Tristem, N. J. and Canning, E. U. (2000). Phylogentic relationships of Pleistophora-like Microsporidia based on small subunit ribosomal DNA sequences and implications for the source of Trachipleistophora hominis infections. The Journal of Eukaryotic Microbiology 47, 280287.CrossRefGoogle Scholar
Diamant, A., Goren, M., Yoke, M. B., Galil, B. S., Klopman, Y., Huchon, D., Szitenberg, A. and Karhan, S. U. (2010). Dasyatispora levantinae gen. et sp. nov., a new microsporidian parasite from the common stingray Dasyatis pastinaca in the eastern Mediterranean. Diseases Aquatic Organisms 91, 137150.CrossRefGoogle Scholar
Egusa, S. (1982). A microsporidian species from yellowtail juveniles, Seriola quinqueradiata, with ‘Beko’ disease. Fish Pathology 16, 187192.CrossRefGoogle Scholar
Faye, A. (1992). Microsporidies des poissons des côtes sénégalaises: faunistique, biologie, ultrastructure. Ph.D. thesis, Université Montpellier II, Sciences et Techniques du Languedoc, France.Google Scholar
Freeman, M. A., Yokoyama, H. and Ogawa, K. (2004). A microsporidian parasite of the genus Spraguea in the nervous tissues of the Japanese anglerfish Lophius litulon. Folia Parasitologica 51, 167176.CrossRefGoogle ScholarPubMed
Guindon, S. and Gascuel, O. (2003). A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology 52, 696704.CrossRefGoogle ScholarPubMed
Leiro, J., Paramá, A., Ortega, M., Santamarina, M. T. and Sanmartin, M. L. (1999). Redescription of Glugea caulleryi, a microsporidian parasite of the greater sand-eel, Hyperoplus lanceolatus (Le sauvage), (Teleostei: Ammodytidae), as Microgemma caulleryi comb. nov. Journal of Fish Diseases 22, 101110.CrossRefGoogle Scholar
Lom, J. (2002). A catalogue of described genera and species of microsporidians parasitic in fish. Systematic Parasitology 53, 8199.CrossRefGoogle ScholarPubMed
Lom, J. and Dyková, I. (1992). Microsporidia (Phylum Microspora Sprague, 1977). In Protozoan Parasites of Fishes. Developments in Aquaculture and Fisheries Science, Vol. 26, (ed. Lom, J. and Dyková, I.), pp. 125157. Elsevier, Amsterdam, The Netherlands.Google Scholar
Lom, J., Dyková, I. and Tonguthai, K. (1999). Kabataia gen. n., a new genus proposed for Microsporidium spp. infecting trunk muscles of fishes. Diseases Aquatic Organisms 38, 3946.CrossRefGoogle Scholar
Lom, J. and Nilsen, F. (2003). Fish Microsporidia: fine structural diversity and phylogeny. International Journal for Parasitology 33, 107127.CrossRefGoogle ScholarPubMed
Mansour, L., Prensier, G., Jemaa, S. B., Hassine, O. K. B., Metenier, G., Vivarès, C. P. and Cornillot, E. (2005). Description of a xenoma-inducing microsporidian, Microgemma tincae n. sp., a parasite of the teleost fish Symphodus tinca from Tunisian coasts. Diseases Aquatic Organisms 65, 217226.CrossRefGoogle Scholar
Matos, E. and Azevedo, C. (2004). Ultrastructural description of Microsporidium brevirostris sp. n., parasite of the teleostean Brachyhypopomus brevirostris (Hypopomidae) from the Amazon River. Acta Protozoologica 43, 261267.Google Scholar
Matthews, R. and Matthews, B. (1980). Cell and tissue reactions of turbot Scophthalmus maximus (L.) to Tetramicra brevifilum gen. n., sp. n. (Microspora). Journal Fish Diseases 3, 495515.CrossRefGoogle Scholar
Miwa, S., Kamaishi, T., Hirae, T., Murase, T. and Nishioka, T. (2011) Encephalomyelitis associated with microsporidian infection in farmed amberjack, Seriola dumerili (Risso). Journal Fish Diseases 34, 901910.CrossRefGoogle ScholarPubMed
Narasimhamurti, C. C. and Sonabai, R. (1977) A new microsporidian Pleistophora carangoidi n. sp. from the body muscles of the marine fish, Carangoides malabaricus. Proceedings of the 5th International Congress on Protozoology, New York, USA, pp. 192.Google Scholar
Nilsen, F. (2000). Small subunit ribosomal DNA phylogeny of Microsporidia with particular reference to genera that infect fish. Journal of Parasitology 86, 128133.CrossRefGoogle ScholarPubMed
Ralphs, J. R. and Matthews, R. A. (1986). Hepatic microsporidiosis of juvenile grey mullet, Chelon labrosus (Risso), due to Microgemma hepaticus gen. nov., sp. nov. Journal Fish Diseases 9, 225242.CrossRefGoogle Scholar
Riley, K. L., Weirich, C. R. and Cerino, D. (2009). Development and growth of hatchery-reared larval Florida pompano (Trachinotus carolinus). Fisheries Bulletin 107, 318328.Google Scholar
Saitou, N. and Nei, M. (1987). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology Evolution 4, 406425.Google Scholar
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. and Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology Evolution 28, 27312739.CrossRefGoogle ScholarPubMed
Thompson, J. D., Higgins, D. G. and Gilson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle ScholarPubMed
Toguebaye, B. S., Marchand, B. and Faye, A. (1989). Preliminary observations on a microsporidian parasite of Chloroscombrus chrysurus Linnaeus, 1776 (Teleost fish). Annales de Parasitologie Humaine et Comparee 64, 157160.CrossRefGoogle 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. The Journal Eukaryotic Microbiology 40, 354362.CrossRefGoogle ScholarPubMed
Vossbrinck, C. R. and Debrunner-Vossbrinck, B. A. (2005). Molecular phylogeny of the Microsporidia: ecological, ultrastructural and taxonomic considerations. Folia Parasitologica 52, 131142.CrossRefGoogle ScholarPubMed