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Mikrocytos Roughleyi Taxonomic Affiliation Leads to the Genus Bonamia (Haplosporidia)

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Mikrocytos Roughleyi Taxonomic Affiliation Leads to the Genus Bonamia (Haplosporidia) DISEASES OF AQUATIC ORGANISMS Vol. 54: 209–217, 2003 Published April 24 Dis Aquat Org Mikrocytos roughleyi taxonomic affiliation leads to the genus Bonamia (Haplosporidia) N. Cochennec-Laureau1, 4,*, K. S. Reece2, F. C. J. Berthe1, P. M. Hine3 1Institut Français de Recherche pour l’Exploitation de la Mer (IFREMER), Laboratoire de Génétique et Pathologie, PO Box 1346, 17390 La Tremblade, France 2Virginia Institute of Marine Science (VIMS), Aquaculture Genetics and Breeding Technology Center, Gloucester Point, Virginia 23062, USA 3Aquatic Animal Diseases, National Centre for Disease Investigation, Ministry of Agriculture and Fisheries (MAF) Operations, PO Box 40-742, Upper Hutt, 6007 Wellington, New Zealand 4Present address: IFREMER, Laboratoire d’Aquaculture Tropicale, BP 7004, 98719 Taravao, French Polynesia ABSTRACT: Microcell-type parasites of oysters are associated with a complex of diseases in different oyster species around the world. The etiological agents are protists of very small size that are very dif- ficult to characterize taxonomically. Associated lesions may vary according to the host species, and their occurrence may be related to variations in tissue structure. Lesion morphology cannot be used to distinguish the different agents involved. Ultrastructural observations on Mikrocytos roughleyi revealed similarities with Bonamia spp., particularly in regard to the presence of electron-dense hap- losporosomes and mitochondria, whose absence from M. mackini also indicate that M. roughleyi and M. mackini are not congeneric. A partial small subunit (ssu) rRNA gene sequence of M. roughleyi was determined. This partial sequence, 951 nucleotides in length, has 95.2 and 98.4% sequence sim- ilarities with B. ostreae and B. exitiosus ssu rDNA sequences, respectively. Polymorphisms among the ssu rDNA sequences of B. ostreae, B. exitiosus and M. roughleyi allowed identification of restriction enzyme digestion patterns diagnostic for each species. Phylogenetic analysis based on the ssu rDNA data suggested that M. roughleyi belongs in the phylum Haplosporidia and that it is closely related to Bonamia spp. On the basis of ultrastructural and molecular considerations, M. roughleyi should be considered a putative member of the genus Bonamia. KEY WORDS: Mikrocytos roughleyi · Saccostrea glomerata · Bonamiosis · Microcell · Taxonomy · Small subunit rDNA Resale or republication not permitted without written consent of the publisher INTRODUCTION 1980, Bannister & Key 1982, Polanco et al. 1984, Elston et al. 1986, McArdle et al. 1991, Barber & Davis 1994), Among the 10 OIE (Office International des Epi- B. exitiosus infects the New Zealand dredge oyster T. zooties: the World Organization for Animal Health)- chilensis (Dinamani et al. 1987, Hine 1991, Hine et al. listed diseases of molluscs, 4 are caused by non-spore- 2001b), and Bonamia-like organisms also infect the flat forming organisms given the collective name of oysters O. angasi in Australia (Hine 1996) and T. chilen- ‘microcell’ (Farley et al. 1988). Of these, 1 disease, sis in Chile (Kern 1993, Campalans et al. 2000) (present bonamiosis, is caused by at least 2 haplosporidian pro- Table 1). A second disease, mikrocytosis, is caused by 2 tozoans that infect the haemocytes of flat oysters. other ‘microcell’ protozoans: Mikrocytos mackini Bonamia ostreae infects the European flat oyster Ostrea causes Denman Island disease in the Pacific oysters edulis in Europe and in North America (Pichot et al. Crassostrea gigas in British Columbia (Quayle 1961, *Email: [email protected] © Inter-Research 2003 · www.int-res.com 210 Dis Aquat Org 54: 209–217, 2003 Table 1. Comparisons among pathogen species, natural and experimental hosts, gross signs, histological features and parasite location. nd: disease experimental reproduction not done Bonamia ostreae Bonamia exitiosus Bonamia sp. Mikrocytos roughleyi M. mackini Natural hosts Ostrea edulis Tiostrea chilensis O. angasi Saccostrea glomerata Crassostrea gigas T. chilensis Experimental hosts O. puelchana nd nd nd C. virginica O. concaphila O. edulis O. angasi O. concaphila T. chilensis C. rivularis Gross signs Gill and mantle No sign No sign Abscesses and Abscesses and perforations or pustules on mantle pustules on mantle indentations or muscle or muscle Histological features Global haemocyte Global haemocyte Global haemocyte Focal haemocyte Focal haemocyte infiltration infiltration infiltration infiltration infiltration Location Haemocytes and Haemocytes Haemocytes Haemocytes Haemocytes, cells epithelial myocytes, connective cells Farley et al. 1988), and M. roughleyi causes winter mor- because of the lack of organelles in most eukaryotic tality in the Sydney rock oyster Saccostrea glomerata in cells including mitochondria or their equivalents (Far- SE Australia (Roughley 1926, Farley et al. 1988). Exper- ley et al. 1988, Hine et al. 2001a). There have been no imentally, Bonamia spp. can infect Ostrea spp. (Grizel published studies on the ultrastructure of M. roughleyi. et al. 1983, Le Borgne & Le Pennec 1983, Bougrier et al. The only Mikrocytos sp. for which sequences from the 1986, Pascual et al. 1991) and C. rivularis (Cochennec et ssu rDNA gene cluster have been published is M. al. 1998). M. mackini has been shown to infect C. gigas, roughleyi (Adlard & Lester 1995). C. virginica, O. edulis and O. concaphila (Bower et al. Certification of stocks as free from specific disease 1997) (present Table 1). Therefore, Bonamia spp. and agents prior to movement is the basis of disease control Mikrocytos spp. cannot be distinguished solely by the in member countries of the Office International des hosts which they infect. However, to date the geo- Epizootis. For this to be effective, listed etiological graphic distributions of the 2 Mikrocytos species ap- agents must be reliably detectable and identifiable. pear to be distinct, with M. mackini having been re- Heavy infection by microcells may be detected by light ported only in western Canada and M. roughleyi only microscopy, but identification cannot be carried out in eastern Australia. with any certainty. Also, light infection cannot reliably Several studies have included observations of the be detected by light or electron microscopy. There is ultrastructure of Bonamia ostreae (Comps et al. 1980, an urgent need to characterize each ‘microcell’ spe- Pichot et al. 1980, Bréhelin et al. 1982, Grizel et al. cies, and identify gene sequences that allow them to be 1983, Grizel 1985, Chagot et al. 1992, Montes et al. distinguished from each other. 1994) and B. exitiosus (Dinamani et al. 1987, Hine The aim of this study was the characterization of 1991, Hine & Wesney 1994a,b, Hine et al. 2001b), but Mikrocytos roughleyi by means of ultrastructural there are none on Bonamia sp. in Ostrea angasi in Aus- observation and ssu rDNA gene sequence determina- tralia or Tiostrea chilensis in Chile. A recent study on tion to clarify taxonomic relationships with other the ssu rDNA gene sequences of B. ostreae (Carnegie microcell parasites. et al. 2000, Cochennec et al. 2000) and Bonamia sp. from New Zealand showed that they are congeneric, and a new species, B. exitiosus, was created (Hine et MATERIALS AND METHODS al. 2001b). An unpublished study on the ssu rDNA gene sequences of Bonamia sp. from Australia and B. Electron microscopy. 4% glutaraldehyde (in 0.2 M exitiosus from New Zealand suggests that these 2 par- cacodylate buffer) fixed tissues from infected Sac- asites are conspecific, despite showing very different costrea glomerata were provided by R. Hand, New pathology in their respective hosts (R. D. Adlard pers. South Wales Australia Fisheries Department. They comm.). were post-fixed for 1 h in 1% osmium tetroxide (OsO4) The ultrastructure of Mikrocytos mackini confirms in 0.2 M cacodylate buffer. Tissues were then cleared that this parasite is different from Bonamia spp. in propylene oxide and embedded in epon resin. Ultra- Cochennec-Laureau et al.: Mikrocytos roughleyi affiliation to Bonamia spp. 211 thin sections were made using copper grids and dou- AF052190; Symbiodinium corculorum: L13717); api- ble-stained with uranyl acetate and lead citrate. These complexans (Babesia bovis: L19078; Theileria parva: were then examined in a Jeol JEM 1200 EX trans- L02366; Eimeria tenella: U40264; Sarcocystis hominis: mission electron microscope. AF006470; Toxoplasma gondii: U03070); ciliates (Eu- DNA extraction. Genomic DNA was extracted from plotes crassus: AY007438; Oxytricha nova: X03948; O. ethanol-fixed, individually infected oysters. Tissues trifallax: AF164121; Entodinium caudatum: U57765; were suspended in 10 volumes of extraction buffer Paramecium tetraurelia: X03772; Tetrahymena pyrifor- (NaCl 100 mM, EDTA 25 mM, pH 8, SDS 0.5%) with mis: M98021; T. thermophila: X56165); fungi (Ajello- Proteinase K (100 µg ml–1). Following overnight incu- myces capsulatus: Z75307; Neurospora crassa: X04971; bation at 50°C, DNA was extracted using a standard Kluyveromyces lactis: X51830; Saccharomyces cere- phenol/chloroform protocol followed by ethanol pre- visiae: J01353; Candida glabrata, X51831; Pneumo- cipitation (Sambrook et al. 1989). cystis carinii: S83267); stramenopiles (Fucus distichus: Polymerase chain reaction. The partial ssu rDNA M97959; Ochromonas danica: M32704; Achlya bisexu- was amplified using the universal primer Suni and the alis: M32705; Phytophthora megasperma: X54265; Bonamia ostreae specific primer Bo-Boas (Cochennec QPX; AF261664; Ulkenia profunda: L34054); haplo- et al. 2000). PCR was performed
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