Ultrastructural and molecular characterization of Haplosporidium montforti n. sp., parasite of the European abalone Haliotis tuberculata

Azevedo, Carlos; Balseiro, Pablo; Casal, Graça; Gestal, Camino; Aranguren, Raquel; Stokes, Nancy A.; Carnegie, Ryan B.; Novoa, Beatriz; Burreson, Eugene M.; Figueras, António

doi:10.1016/j.jip.2006.02.002

Cited by 36 publications

(25 citation statements)

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“…These prokaryotes have been reported from marine animals (Lauckner 1983), mainly crustaceans (Bonami & Pappalardo 1980, Fryer & Lannan 1994, Nunan et al 2003 and bivalves (Buchannan 1978, Elston 1986, Azevedo & Villalba 1991, Gardner et al 1995, Hine & Diggles 2002, Azevedo et al 2005. Previous studies on bivalves infected with rickettsia or RLOs have demonstrated that these prokaryotes can cause important losses in commercially farmed bivalves (Gardner et al 1995, Bower 2004.The ultrastructural organization of the compacted chromatin of the RLOs studied in the present work differs from all the other rickettsia and RLOs previously described in molluscs (Elston 1986, Azevedo & Villalba 1991, Gardner et al 1995, Azevedo et al 2005.The RLOs described in the present paper were found coincidentally in tissues of cultured Haliotis tuberculata which had experienced high mortality possibly due to the presence of a haplosporidian infection identified as Haplosporidium montforti (Azevedo et al 2006). During an ultrastructural study of a recently identified haplosporidian found among cultured abalone Haliotis iris, rickettsiae were also encountered and associated with the mortality of the host .…”

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Ultrastructural description of new Rickettsia-like organisms in the commercial abalone Haliotis tuberculata (Gastropoda: Haliotidae) from the NW of Spain

Azevedo¹,

Conchas²,

Tajdari³

et al. 2006

Dis. Aquat. Org.

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Rickettsia-like organisms (RLOs) were found in the commercially farmed abalone Haliotis tuberculata in the northwestern region of the Atlantic Coast of Spain and are described from light and transmission electron microscopy observations. The RLOs measured ~1.6 × 0.9 µm and were found in intracytoplasmic, spherical to ellipsoidal vacuoles (up to 8 µm) in the epithelial cells of the digestive diverticulae. The morphological ultrastructure of these organisms was typically prokaryotic, including a plasmalemma and a thin Gram-negative type cell wall. Several ultrastructural changes were observed in the epithelial cells of the host containing the RLOs. The nuclei became pycnotic and several basophilic dense inclusions appeared in the cytoplasm. In addition, the host cell appeared lysed and was ruptured in advanced stages of infection. It was impossible to ascertain whether the RLOs are responsible for this disease, as a haplosporidian infection was also present. We can only conclude that the presence of RLOs simultaneously with a haplosporidian parasite may contribute to the mortality of the abalone host.KEY WORDS: Ultrastructure · Rickettsia-like organisms · Abalone · Spain Resale or republication not permitted without written consent of the publisherDis Aquat Org 71: [233][234][235][236][237] 2006 cultured and natural populations of Haliotis spp. from different geographic areas (Antonio et al. 2000, Bower 2004. Recently, the syndrome has been described as a severe pathogen-caused disease associated with Rickettsiales-like prokaryotes (Haaker et al. 1992, Gardner et al. 1995, Antonio et al. 2000, Bower 2004, Braid et al. 2005.The purpose of this work is to document and describe the ultrastructure of RLOs found in abalone Haliotis tuberculata. These prokaryotic parasites may contribute to the mortality of this commercially important species. MATERIALS AND METHODSJuvenile abalone Haliotis tuberculata (Linnaeus, 1758) (Gastropoda: Haliotidae) from Ireland were grown in barrels suspended from rafts in El Grove, Galicia, NW of Spain (42°29' 20'' N, 08°53' 56'' W). Fifteen specimens were observed by light microscopy (LM) during a study which aimed to identify haplosporidiosis. In addition to the haplosporidian parasite, some of the specimens were also found to be parasitized by RLOs, mainly in the epithelial cells of the digestive diverticulae.Small fragments of the parasitized tissues were fixed in 3% glutaraldehyde in 0.2 M sodium cacodylate buffer pH 7.2 for 10 h at 4°C, washed overnight in the same buffer at 4°C, and post-fixed in buffered 2% OsO 4 for 3 h at 4°C. After dehydration in an ascendant ethanol series followed by propylene oxide, the tissues were embedded in Epon. Semithin sections were stained with methylene blue-Azur II and observed under differential interference contrast (DIC; Nomarski) microscopy. For transmission electron microscopy (TEM), the tissues were ultrathin-sectioned with a diamond knife, double-stained with uranyl acetate and lead citrate and observed in a JEOL 100CXII TEM operat...

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confidence: 46%

“…Of the 10 specimens of the abalone Haliotis tuberculata parasitized by a haplosporidian identified as Haplosporidium montforti (Azevedo et al 2006), only 6 revealed a simultaneous infection by rickettsia-like organisms (RLOs) (Fig. 1).…”

Section: Resultsmentioning

confidence: 99%

Ultrastructural description of new Rickettsia-like organisms in the commercial abalone Haliotis tuberculata (Gastropoda: Haliotidae) from the NW of Spain

Azevedo¹,

Conchas²,

Tajdari³

et al. 2006

Dis. Aquat. Org.

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“…However, these parasites lacked the distinctive axe-shaped internal membranes observed within the haplosporosomes of the pearl oyster parasite. In addition, Haplosporidium montforti described infecting the abalone Haliotis tuberculata in Spain, has 4 filaments, 20-28 mm long, with 2 attached opposite each other at the basal end and 2 other opposing filaments attached at the apical end of the spore (Azevedo et al 2006). Also, the filaments of the pearl oyster parasite are round in transverse section rather than the L,T or X-like sections of H. montfordi (Azevedo et al 2006).…”

Section: Discussionmentioning

confidence: 99%

“…In addition, Haplosporidium montforti described infecting the abalone Haliotis tuberculata in Spain, has 4 filaments, 20-28 mm long, with 2 attached opposite each other at the basal end and 2 other opposing filaments attached at the apical end of the spore (Azevedo et al 2006). Also, the filaments of the pearl oyster parasite are round in transverse section rather than the L,T or X-like sections of H. montfordi (Azevedo et al 2006). Haplosporidium pickfordi from fresh water snails in the great lakes region of the United States, has 2 posterior knob-like thickenings like the pearl oyster parasite but has approximately 9 filaments wound around the spore rather than the 2 filaments observed here (Burreson, 2001).…”

Section: Discussionmentioning

confidence: 99%

Spore ornamentation of Haplosporidium hinei n. sp. (Haplosporidia) in pearl oysters Pinctada maxima (Jameson, 1901)

et al. 2008

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An infection of pearl oysters, Pinctada maxima, attributed to a Haplosporidium sp. by Hine and Thorne (1998) has been detected on 3 occasions and is considered to represent a serious concern to the pearling industry in Australia. The spore ornamentation of the parasite was determined by scanning electron microscopy and transmission electron microscopy. Spores of the parasite were pleomorphic, or elongated 3 . 5-4 mmr2 . 5-3 . 0 mm in size. Two filaments were wound around the spore and originated from 2 ' knob-like ' posterior thickenings. Both filaments passed up one side of the spore together until just below the operculum whereupon each split and passed obliquely under the lip of the opercula lid. Each filament wrapped around the spore 4 times. The posterior thickenings seem to appear late in the development of the spore and were composed of spore wall material. A second set of branching tubular filaments composed of a different material was observed on the spore body although not on mature spores possessing a ' knob-like ' posterior thickening. The ornamentation on the spores of the pearl oyster parasite was unique amongst described haplosporidian species where spore ornamentation is known. The parasite is named in this manuscript as Haplosporidium hinei n. sp.

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“…European abalone stocks are currently threatened by several pathogens causing severe mass mortalities in wild or farmed populations, among them Xenohaliotis californiensis, Haplosporidium sp. and Vibrio harveyi Azevedo et al 2006;Balseiro et al 2006;Huchette and Clavier 2004).…”

Section: Introductionmentioning

confidence: 99%

Characterization of abalone Haliotis tuberculata–Vibrio harveyi interactions in gill primary cultures

Pichon

Cudennec

Huchette³

et al. 2013

Cytotechnology

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The decline of European abalone Haliotis tuberculata populations has been associated with various pathogens including bacteria of the genus Vibrio. Following the summer mortality outbreaks reported in France between 1998 and 2000, Vibrio harveyi strains were isolated from moribund abalones, allowing in vivo and in vitro studies on the interactions between abalone H. tuberculata and V. harveyi. This work reports the development of primary cell cultures from abalone gill tissue, a target tissue for bacterial colonisation, and their use for in vitro study of host cell-V. harveyi interactions. Gill cells originated from four-day-old explant primary cultures were successfully sub-cultured in multi-well plates and maintained in vitro for up to 24 days. Cytological parameters, cell morphology and viability were monitored over time using flow cytometry analysis and semi-quantitative assay (XTT). Then, gill cell cultures were used to investigate in vitro the interactions with V. harveyi. The effects of two bacterial strains were evaluated on gill cells: a pathogenic bacterial strain ORM4 which is responsible for abalone mortalities and LMG7890 which is a nonpathogenic strain. Cellular responses of gill cells exposed to increasing concentrations of bacteria were evaluated by measuring mitochondrial activity (XTT assay) and phenoloxidase activity, an enzyme which is strongly involved in immune response. The ability of gill cells to phagocyte GFP-tagged V. harveyi was evaluated by flow cytometry and gill cells-V. harveyi interactions were characterized using fluorescence microscopy and transmission electron microscopy. During phagocytosis process we evidenced that V. harveyi bacteria induced significant changes in gill cells metabolism and immune response. Together, the results showed that primary cell cultures from abalone gills are suitable for in vitro study of host-pathogen interactions, providing complementary assays to in vivo experiments.

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Ultrastructural and molecular characterization of Haplosporidium montforti n. sp., parasite of the European abalone Haliotis tuberculata

Cited by 36 publications

References 36 publications

Ultrastructural description of new Rickettsia-like organisms in the commercial abalone Haliotis tuberculata (Gastropoda: Haliotidae) from the NW of Spain

Ultrastructural description of new Rickettsia-like organisms in the commercial abalone Haliotis tuberculata (Gastropoda: Haliotidae) from the NW of Spain

Spore ornamentation of Haplosporidium hinei n. sp. (Haplosporidia) in pearl oysters Pinctada maxima (Jameson, 1901)

Characterization of abalone Haliotis tuberculata–Vibrio harveyi interactions in gill primary cultures

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