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Tetractinomyxon stages genetically consistent with Sphaerospora dicentrarchi (Myxozoa: Sphaerosporidae) found in Capitella sp. (Polychaeta: Capitellidae) suggest potential role of marine polychaetes in parasite's life cycle

Published online by Cambridge University Press:  04 April 2016

LUIS F. RANGEL ,
RICARDO CASTRO ,
SÓNIA ROCHA ,
RICARDO SEVERINO ,
GRAÇA CASAL ,
CARLOS AZEVEDO ,
FRANCISCA CAVALEIRO  and
MARIA J. SANTOS
LUIS F. RANGEL*
Affiliation:
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, Edifício FC4, 4169-007 Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal
RICARDO CASTRO
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal
SÓNIA ROCHA
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira no 228, 4050-313 Porto, Portugal
RICARDO SEVERINO
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal
GRAÇA CASAL
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal Department of Sciences, Institute University of Health Sciences, CESPU, Rua Central da Gandra, 1317, 4585-116 Gandra, Portugal
CARLOS AZEVEDO
Affiliation:
Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal Laboratory of Cell Biology, Institute of Biomedical Sciences Abel Salazar (ICBAS), University of Porto, Rua Jorge Viterbo Ferreira no 228, 4050-313 Porto, Portugal Zoology Department, College of Sciences, King Saud University, 11451 Riyadh, Saudi Arabia
FRANCISCA CAVALEIRO
Affiliation:
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, Edifício FC4, 4169-007 Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal
MARIA J. SANTOS
Affiliation:
Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, Edifício FC4, 4169-007 Porto, Portugal Interdisciplinary Centre of Marine and Environmental Research (CIIMAR/CIMAR), University of Porto, Rua dos Bragas 289, 4050-123 Porto, Portugal
*
*Corresponding author: Department of Biology, Faculty of Sciences, University of Porto, Rua do Campo Alegre, s/n, Edifício FC4, 4169-007 Porto, Portugal. E-mail: luisfiliperangel@sapo.pt
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Summary

Known life cycles of myxosporean parasites have two hosts, but very few life cycles have been disclosed, especially in the marine environment. Sphaerospora dicentrarchi Sitjà-Bobadilla and Álvarez-Pellitero, 1992 is a systemic parasite from the European seabass, Dicentrarchus labrax (Linnaeus, 1758), a highly valuable commercial fish. It affects its health, leading to aquaculture production losses. During 2013 and 2014, an actinospore survey was conducted in a total of 5942 annelids collected from a fish farm in Algarve and from the Aveiro Estuary, in Portugal. A new tetractinomyxon actinospore was found in a capitellid polychaete, belonging to the genera Capitella collected at the fish farm. The tetractinomyxons were pyriform measuring 11·1 ± 0·7 µm in length and 7·2 ± 0·4 µm in width, and presented three rounded polar capsules measuring 2·4 ± 0·3 µm in diameter. The molecular analysis of the 18S rRNA gene sequences from the tetractinomyxons revealed a similarity of 100% with the DNA sequences deposited in the GenBank from S. dicentrarchi myxospores collected from the European seabass and the spotted seabass in the same fish farm and 99·9% similarity with the DNA sequence obtained from the myxospores found infecting the European seabass in the Aveiro Estuary. Therefore, the new tetractinomyxons are inferred to represent the actinospore phase of the S. dicentrarchi life cycle.

Keywords

Sphaerospora dicentrarchilife cyclePolychaetaCapitella sp.tetractinomyxonPortugal
Type
Research Article
Information
Parasitology , Volume 143 , Issue 8 , July 2016 , pp. 1067 - 1073
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Copyright
Copyright © Cambridge University Press 2016 

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References

REFERENCES

Azevedo, C., Casal, G., Garcia, P., Matos, P., TelesGrilo, L. and Matos, E. (2009). Ultrastructural and phylogenetic data of Chloromyxum riorajum sp. nov. (Myxozoa), a parasite of the stingray Rioraja agassizii in Southern Brazil. Diseases of Aquatic Organisms 85, 41–51.Google Scholar
Bartholomew, J. L., Whipple, M. J., Stevens, D. G. and Fryer, J. L. (1997). The life cycle of Ceratomyxa shasta, a myxosporean parasite of salmonids, requires a freshwater polychaete as an alternate host. Journal of Parasitology 83, 859–868.CrossRefGoogle ScholarPubMed
Bartholomew, J. L., Atkinson, S. D. and Hallett, S. L. (2006). Involvement of Manayunkia speciosa (Annelida: Polychaeta: Sabellidae) in the life cycle of Parvicapsula minibicornis, a myxozoan parasite of Pacific salmon. Journal of Parasitology 92, 742–748.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.Google Scholar
Bartošová, P., Freeman, M. A., Yokoyama, H., Caffara, M. and Fiala, I. (2011). Phylogenetic position of Sphaerospora testicularis and Latyspora scomberomori n. gen. n. sp. (Myxozoa) within the marine urinary clade. Parasitology 138, 381–393.Google Scholar
Blake, J. A. (2009). Redescription of Capitella capitata (Fabricius) from West Greenland and designation of a neotype (Polychaeta, Capitellidae). Zoosymposia 2, 55–80.Google Scholar
Blake, J. A., Grassle, J. P. and Eckelbarger, K. J. (2009). Capitella teleta, a new species designation for the opportunistic and experimental Capitella sp. I, with a review of the literature for confirmed records. Zoosymposia 2, 25–53.Google Scholar
Cabral, H. and Costa, M. J. (2001). Abundance, feeding ecology and growth of 0-group sea bass, Dicentrarchus labrax, within the nursery areas of the Tagus estuary. Journal of the Marine Biological Association of the United Kingdom 81, 679–682.CrossRefGoogle Scholar
Costa, M. J. (1988). The Tagus and Mira estuaries (Portugal) and their role as spawning and nursery areas. Journal of Fish Biology 33(Suppl. sA), 249–250.CrossRefGoogle Scholar
Diamant, A. (1997). Fish-to-fish transmission of a marine myxosporean. Diseases of Aquatic Organisms 30, 99–105.CrossRefGoogle Scholar
Diamant, A., Ucko, M., Paperna, I., Colorni, A. and Lipshitz, A. (2005). Kudoa iwatai (Myxosporea: Multivalvulida) in wild and cultured fish in the Red Sea: redescription and molecular phylogeny. Journal of Parasitology 91, 1175–1189.Google Scholar
Dyková, I., Buron, I., Fiala, I. and Roumillat, W. A. (2009). Kudoa inornata sp.n. (Myxosporea: Multivalvulida) from the skeletal muscles of Cynoscion nebulosus (Teleostei: Sciaenidae). Folia Parasitologica 56, 91–98.CrossRefGoogle ScholarPubMed
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.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.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 seabass (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.Google Scholar
Grassle, J. and Grassle, J. F. (1976). Sibling species in the marine pollution indicator Capitella (polychaeta). Science 192, 567–569.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
Hampel, H., Cattrijsse, A. and Elliott, M. (2005). Feeding habits of young predatory fishes in marsh creeks situated along the salinity gradient of the Schelde estuary, Belgium and The Netherlands. Helgoland Marine Research 59, 151–162.Google Scholar
Hillis, D. M. and Dixon, M. T. (1991). Ribosomal DNA: molecular evolution and phylogenetic inference. Quarterly Review of Biology 66, 411–453.CrossRefGoogle ScholarPubMed
Ikeda, I. (1912). Studies on some sporozoan parasites of sipunculoids. I. The life-history of a new actinomyxidian, Tetractinomyxon intermedium g. et sp. nov. Archiv für Protistenkunde 25, 240–272.Google Scholar
Karlsbakk, E. and Køie, M. (2012). The marine myxosporean Sigmomyxa sphaerica (Thélohan, 1895) gen. n., comb. n. (syn. Myxidium sphaericum) from garfish (Belone belone (L.)) uses the polychaete Nereis pelagica L. as invertebrate host. Parasitology Research 110, 211–218.Google Scholar
Køie, M. (2000). First record of an actinosporean (Myxozoa) in a marine polychaete annelid. Journal of Parasitology 86, 871–872.Google Scholar
Køie, M. (2002). Spirorbid and serpulid polychaetes are candidates as invertebrate hosts for Myxozoa. Folia Parasitologica 49, 160–162.Google Scholar
Køie, M. (2005). The Spionidae (Polychaeta) act as invertebrate hosts for marine Myxozoa. European Association of Fish Pathologists 25, 179–181.Google Scholar
Køie, M., Whipps, C. M. and Kent, M. L. (2004). Ellipsomyxa gobii (Myxozoa: Ceratomyxidae) in the common goby Pomatoschistus microps (Teleostei: Gobiidae) uses Nereis spp. (Annelida: Polychaeta) as invertebrate hosts. Folia Parasitologica 51, 14–18.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
Køie, M., Karlsbakk, E. and Nylund, A. (2008). The marine herring myxozoan Ceratomyxa auerbachi (Myxozoa: Ceratomyxidae) uses Chone infundibuliformis (Annelida: Polychaeta: Sabellidae) as invertebrate host. Folia Parasitologica 55, 100–104.Google Scholar
Køie, M., Karlsbakk, E., Einen, A.-C. B. and Nylund, A. (2013). A parvicapsulid (Myxozoa) infecting Sprattus sprattus and Clupea harengus (Clupeidae) in the Northeast Atlantic uses Hydroides norvegicus (Serpulidae) as invertebrate host. Folia Parasitologica 60, 149–154.Google Scholar
Laffaille, P., Lefeuvre, J.-C., Schricke, M.-T. and Feunteun, E. (2001). Feeding ecology of 0-group sea bass, Dicentrarchus labrax, in salt marshes of Mont Saint Michel Bay (France). Estuaries 24, 116–125.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.Google Scholar
Lom, J. and Dyková, I. (2006). Myxozoan genera: definition and notes on taxonomy, life-cycle terminology and pathogenic species. Folia Parasitologica 53, 1–36.Google Scholar
Lom, J., McGeorge, J., Feist, S. W., Morris, D. and Adams, A. (1997). Guidelines for the uniform characterisation of the actinosporean stages of parasites of the phylum Myxozoa. Diseases of Aquatic Organisms 30, 1–9.Google Scholar
Martin, D. and Grémare, A. (1997). Secondary production of Capitella sp. (Polychaeta: Capitellidae) inhabiting different organically enriched environments. Scientia Marina 61, 99–109.Google Scholar
Martin, J. P. and Bastida, R. (2006). Life history and production of Capitella capitata (Polychaeta: Capitellidae) in Río de la Plata Estuary (Argentina). Thalassas 22, 25–38.Google Scholar
Martinho, F., Leitão, R., Neto, J. M., Cabral, H., Lagardère, F. and Pardal, M. A. (2008). Estuarine colonization, population structure and nursery functioning for 0-group sea bass (Dicentrarchus labrax), flounder (Platichthys flesus) and sole (Solea solea) in a mesotidal temperate estuary. Journal of Applied Ichthyology 24, 229–237.Google Scholar
Méndez, N., Linke-Gamenick, I. and Forbes, V. E. (2000). Variability in reproductive mode and larval development within the Capitella capitata species complex. Invertebrate Reproduction and Development 38, 131–142.CrossRefGoogle Scholar
Merella, P., Garippa, G. and Salati, F. (2006). Parasites of cage cultured European seabass Dicentrarchus labrax and gilthead seabream Sparus aurata from Sardinia (western Mediterranean): first results. Parassitologia 48, 290.Google Scholar
Mladineo, I. (2003). Myxosporidean infections in Adriatic cage-reared fish. Bulletin of the European Association of Fish Pathologists 23, 113–122.Google Scholar
Mladineo, I., Petrić, M., Šegvić, T. and Dobričić, N. (2010). Scarcity of parasite assemblages in the Adriatic-reared European sea bass (Dicentrarchus labrax) and sea bream (Sparus aurata). Veterinary Parasitology 174, 131–138.Google Scholar
Morris, D. J. (2012). A new model for myxosporean (Myxozoa) development explains the endogenous budding phenomenon, the nature of cell within cell life stages and evolution of parasitism from a cnidarian ancestor. International Journal for Parasitology 42, 829–840.Google 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.Google Scholar
Palumbi, S., Martin, A., Romano, S., McMillan, W. O., Stice, L. and Grabowski, G. (2002). The Simple Fool's Guide to PCR. Version 2.0. 45 p.Google Scholar
Pickett, G. D. and Pawson, M. G. (1994). Sea bass. Biology, Exploitation and Conservation. Chapman & Hall, London, 337 p.Google Scholar
Rangel, L. F., Santos, M. J., Cech, G. and Székely, C. (2009). Morphology, molecular data, and development of Zschokkella mugilis (Myxosporea, Bivalvulida) in a polychaete alternate host, Nereis diversicolor. Journal of Parasitology 95, 561–569.Google Scholar
Rangel, L. F., Cech, G., Székely, C. and Santos, M. J. (2011). A new actinospore type Unicapsulactinomyxon (Myxozoa), infecting the marine polychaete, Diopatra neapolitana (Polychaeta: Onuphidae) in the Aveiro Estuary (Portugal). Parasitology 138, 698–712.CrossRefGoogle ScholarPubMed
Rangel, L. F., Rocha, S., Castro, R., Severino, R., Casal, G. and Santos, M. J. (2015 a). A new type of Echinactinomyxon (Myxozoa), infecting a marine polychaete, Heteromastus filiformis (Polychaeta: Capitellidae) in the Alvor Estuary (Portugal). Microscopy and Microanalysis 21, 85–86.Google Scholar
Rangel, L. F., Rocha, S., Castro, R., Severino, R., Casal, G., Azevedo, C., Cavaleiro, F. and Santos, M. J. (2015 b). The life cycle of Ortholinea auratae (Myxozoa: Ortholineidae) involves an actinospore of the triactinomyxon morphotype infecting a marine oligochaete. Parasitology Research 114, 2671–2678.Google Scholar
Santos, M. J. (1998). Parasitas do robalo (Dicentrarchus labrax L.) da Ria de Aveiro e sua dinâmica populacional. Ph.D. thesis. University of Porto, 261 p.Google Scholar
Sitjà-Bobadilla, A. and Álvarez-Pellitero, P. (1992). Light and electron microscopic description of Sphaerospora dicentrarchi n. sp. (Myxosporea: Sphaerosporidae) from wild and cultured sea bass, Dicentrarchus labrax L. Journal of Eukaryotic Microbiology 39, 273–281.Google Scholar
Sitjà-Bobadilla, A. and Álvarez-Pellitero, P. (1993). Population dynamics of Sphaerospora dicentrarchi Sitja-Bobadilla et Alvarez-Pellitero, 1992 and S. testicularis Sitja-Bobadilla et Alvarez-Pellitero, 1990 (Myxosporea: Bivalvulida) infections in wild and cultured Mediterranean sea bass (Dicentrarchus labrax L.). Parasitology 106, 39–45.Google Scholar
Spitz, J., Chouvelon, T., Cardinaud, M., Kostecki, C. and Lorance, P. (2013). Prey preferences of adult sea bass Dicentrarchus labrax in the northeastern Atlantic: implications for bycatch of common dolphin Delphinus delphis. ICES Journal of Marine Science 70, 452–461.CrossRefGoogle Scholar
Székely, C., Borkhanuddin, M. H., Cech, G., Kelemen, O. and Molnár, K. (2014). Life cycles of three Myxobolus spp. from cyprinid fishes of Lake Balaton, Hungary involve triactinomyxon-type actinospores. Parasitology Research 113, 2817–2825.Google Scholar
Tsutsumi, H. (1990). Population persistence of Capitella sp (Polychaeta; Capitellidae) on a mud flat subject to environmental disturbance by organic enrichment. Marine Ecology Progress Series 63, 147–156.Google Scholar
Tsutsumi, H., Fukunaga, S., Fujita, N. and Sumida, M. (1990). Relationship between growth of Capitella sp. and organic enrichment of the sediment. Marine Ecology Progress Series 63, 157–162.Google Scholar
Warren, L. M. (1976). A population study of the polychaete Capitella capitata at plymouth. Marine Biology 38, 209–216.Google Scholar
Whipps, C. M., Adlard, R. D., Bryant, M. S., Lester, R. J. G., Findlav, V. and Kent, M. L. (2003). First report of three Kudoa species from Eastern Australia: Kudoa thyrsites from Mahi mahi (Coryphaena hippurus), Kudoa amamiensis and Kudoa minithyrsites n. sp. from sweeper (Pempheris ypsilychnus). Journal of Eukaryotic Microbiology 50, 215–219.Google Scholar
Xavier, R., Severino, R., Pérez-Losada, M., Cable, J. and Harris, D. J. (2013). First record of Sphaerospora dicentrarchi (Myxosporea, Sphaerosporidae) in Dicentrarchus punctatus. Bulletin of the European Association of Fish Pathologists 33, 21–23.Google Scholar
Yokoyama, H., Grabner, D. and Shirakashi, S. (2012). Transmission biology of the Myxozoa. In Health and Environment in Aquaculture (ed. Carvalho, E.), pp. 3–42. InTech. ISBN: 978-953-51-0497-1, doi: 10.5772/29571; Available from: http://www.intechopen.com/books/health-and-environment-in-aquaculture/transmission-biology-of-the-myxozoaGoogle Scholar