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Pathogenicity of Miamiensis Avidus (Syn. Philasterides Dicentrarchi

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Pathogenicity of Miamiensis Avidus (Syn. Philasterides Dicentrarchi Vol. 83: 133–143, 2009 DISEASES OF AQUATIC ORGANISMS Published February 12 doi: 10.3354/dao02017 Dis Aquat Org Pathogenicity of Miamiensis avidus (syn. Philasterides dicentrarchi), Pseudocohnilembus persalinus, Pseudocohnilembus hargisi and Uronema marinum (Ciliophora, Scuticociliatida) Jun-Young Song1, Shin-Ichi Kitamura1, 4, Myung-Joo Oh1, Hyun-Sil Kang2, Je-hee Lee2, Shin-Ji Tanaka3, Sung-Ju Jung1,* 1Department of Aqualife Medicine, Chonnam National University, Chonnam 550-749, South Korea 2Department of Marine Biotechnology, Cheju National University, Jeju-Do 690-756, South Korea 3Fisheries Research Division, Mie Prefectural Science and Technology Promotion Center, Mie 517-0404, Japan 4Present address: Center for Marine Environmental Studies (CMES), Ehime University, Bunkyo-cho 3, Matsuyama 790-8577, Japan ABSTRACT: The scuticociliates Miamiensis avidus (syn. Philasterides dicentrarchi), Pseudocohni- lembus persalinus, Pseudocohnilembus hargisi and Uronema marinum were cloned and identified using morphological characteristics and the small subunit ribosomal RNA gene (SSU rRNA). M. avidus strains YS1, WS1, YK1 and JJ3 from southern coastal areas and Jeju Island in Korea were pathogenic to olive flounder Paralichthys olivaceus (80 to 100% mortality in 8 to 10 g fish) when inoc- ulated intraperitoneally (i.p.) with 1.0 to 1.4 × 106 ciliates fish–1. Mortality was lower (10 to 45%) when the inoculum was 1.0 to 1.4 × 104 ciliates fish–1 in the i.p.-injected group. The M. avidus strains of YS1, WS1, YK1 and JJ3 caused 60 to 100% mortality by immersion infection with 3.2 to 4.2 × 103 ml–1 in 8 to 10 g fish and 3.0 to 4.0 × 103 ml–1 in 30 to 40 g fish. M. avidus strain Mie0301 from the Mie pre- fecture in Japan caused 70% mortality by immersion infection with 4.4 × 103 ml–1 in 30 to 40 g fish. The predominant sign was severe abdominal distension in i.p.-injected fish, and extensive ulcer lesions in the skeletal muscle in immersion-infected fish. Numerous ciliates were observed in the ascetic fluid, ulcers, haemorrhagic lesions, gills and brain of infected fish. However, P. persalinus (strain SCL-A), P. hargisi (strain SCL-B) and U. marinum (strain JK3) showed less than 30% mortal- ity from both i.p. and immersion challenges, with no ciliate invasion in the skin, gills or brain. M. avidus-infected fish showed many ciliates in gills, fins, skin muscle, brain and intestine accompanied by necrosis and haemorrhages. However, no histological changes were observed in P. persalinus-, P. hargisi- or U. marinum-infected fish. KEY WORDS: Pathogenicity · Scuticociliatida · Miamiensis avidus · Philasterides dicentrarchi · Pseudocohnilembus persalinus · Pseudocohnilembus hargisi · Uronema marinum · Olive flounder · Paralichthys olivaceus Resale or republication not permitted without written consent of the publisher INTRODUCTION Kim et al. 2004a,b, Jung et al. 2005), turbot Scophthal- mus maximus (Dyková & Figueras 1994, Sterud et al. Scuticociliates are regarded as serious pathogens in 2000, Iglesias et al. 2001, Puig et al. 2007), sea bass marine aquaculture worldwide. They cause mass mor- Dicentrarchus labrax (Dragesco et al. 1995), southern talities in fish such as olive flounder Paralichthys oli- bluefin tuna Thunnus maccoyii (Munday et al. 1997), vaceus (Yoshinaga & Nakazoe 1993, Jee et al. 2001, seahorse Hippocampus erectus (Thompson & Moewus *Corresponding author. Email: [email protected] © Inter-Research 2009 · www.int-res.com 134 Dis Aquat Org 83: 133–143, 2009 1964) and silver pomfret Pampus argenteus (Azad et Culture. The brain and skin ulcer lesions of infected al. 2007). fish were dissected and washed 3 times in EMEM con- Commercially significant occurrences of scuticocil- taining antibiotics (500 IU ml–1 penicillin and 500 µg iatosis in olive flounder in Korea were first noted in streptomycin). A small piece of tissue was inoculated 1990 (Chun 2000). The ciliates occurred in the gills, into 25 cm2 tissue-culture flasks with Chinook salmon skin, heart, brain, muscles and visceral organs includ- embryo (CHSE-214) cells. The CHSE-214 cells were ing the intestine. Scuticociliatosis is highly histo- cultured in EMEM, supplemented with 10% fetal phagous and destroys infected tissues. The causative bovine serum (FBS), penicillin (50 IU ml–1) and strepto- agents of scuticociliatosis in the olive flounder in Korea mycin (50 µg ml–1) at 20°C. The antibiotic concentra- with the same clinical signs mentioned above have tion was increased 10 times for skin samples (500 IU been isolated and identified as Uronema marinum (Jee ml–1 penicillin and 500 µg ml–1 streptomycin). An iso- et al. 2001), Pseudocohnilembus persalinus (Kim et al. late (JK3) was originated from rotifers, which are a 2004b), Philasterides dicentrarchi (Kim et al. 2004a) food organism for olive flounder larvae. Rotifers con- and Miamiensis avidus (Jung et al. 2005). In addition, a taining scuticociliates were inoculated into 25 cm2 tis- very similar disease with high mortality caused by an sue-culture flasks with CHSE-214 cells supplemented unidentified scuticociliate in olive flounder juveniles with 10 times the antibiotic concentrations. was also reported in Japan (Yoshinaga & Nakazoe Cloning. After 3 to 7 d of culture, each isolate was 1993). However, it is not clear if all the species of scu- cloned 5 times using the limiting dilution method with ticociliates cause mortalities with similar clinical signs some modifications (Goding 1993). Briefly, a series of in olive flounder. dilutions was made from the original culture and cell In a previous study, using small subunit ribosomal numbers were adjusted to a concentration of 10 ciliates RNA gene (SSU rRNA) and morphological characteris- ml–1. Then, 50 µl of the diluted suspension was inocu- tics, we confirmed Miamiensis avidus as a senior syn- lated into each well (0.5 cells well–1) of a 96 well tissue- onym of Philasterides dicentrarchi (Jung et al. 2007). culture plate containing 100 µl of CHSE-214 cell sus- Moreover, pathogenicity of the M. avidus YS1 strain pension. was confirmed by experimental infections. In the pre- Identification. Morphological studies were made sent study, we experimentally infected olive flounder using the silver carbonate and ‘wet’ silver nitrate meth- with M. avidus, Uronema marinum, Pseudocohnilem- ods described by Foissner (1991). For the silver carbon- bus persalinus and Pseudocohnilembus hargisi to ate stain, ciliates were fixed in 5% formalin, washed determine their pathogenicity; results suggest that M. and then stained in Fernandez-Galiano’s fluid on a avidus is the main cause of mortality in olive flounder. pre-heated (60°C) hot plate approximately 5 min until the solution turned golden brown. The reaction was terminated using 5% sodium thiosulfate. For the silver MATERIALS AND METHODS nitrate stain, concentrated ciliates were fixed in cen- trifuge tubes with Champy’s fixative, and then washed Ciliate collection. Scuticociliates were isolated from into DaFano’s fixative. Slides were warmed on a slide 7 olive flounder at different farms. One strain (JK3) warmer set at 35 to 45°C. A tiny drop of concentrated was isolated from the rotifer Brachionus plicatilis in an ciliate was placed on a warm slide and embedded in a olive flounder hatchery (Table 1). All infected fish thin gelatin layer. The liquefied preparation was solid- showed typical signs of scuticociliatosis such as severe ified by cooling on a moist cold surface and then rinsed ulcers and haemorrhages in the skeletal muscle. with distilled water. Slides were placed in a cold 3% Table 1. Scuticociliates isolated from olive flounder used in the infection experiments. Uronema marinum was isolated from the rotifer Brachionus plicatilis in an olive flounder hatchery. Dates are given as dd/mm/yyyy Species Strain Sampling date Sampling location Isolated origin Miamiensis avidus YS1 22/05/1999 Yosu Brain WS1 20/08/2003 Wando Brain YK1 26/11/2003 Youngkwang Brain JJ3 29/07/2004 Jeju Brain Mie0301 28/11/2003 Owase Brain Pseudocohnilembus persalinus SCL-A 21/10/2003 Wando Skin ulcer Pseudocohnilembus hargisi SCL-B 21/10/2003 Wando Skin ulcer Uronema marinum JK3 05/08/2004 Jeju Rotifer Song et al.: Pathogenicity of scuticociliates 135 silver nitrate bath for 1 h. After washing with cold dis- Five randomly selected fish were confirmed to be free tilled water, slides were irradiated for 3 to 5 h using from pathogens; the absence of parasites was con- ultraviolet lights on a clean bench until the gelatin firmed by microscopic observation, bacteria by iso- turned golden brown. Slides were subsequently dehy- lation on brain heart infusion agar (BHIA) (Difco) and drated, cleared and mounted. viruses by isolation in CHSE-214 cells. Fish were held SSU rRNA analysis was carried out as described pre- in laboratory conditions for 10 d until experimental viously (Jung et al. 2005). Briefly, 1 ml of cultured cili- infection. Water was maintained at approximately ates was harvested by centrifugation at 2000 × g for 20°C, and was constantly aerated for the duration of 5 min. The pellet was lysed in a solution of 170 µl Tris- the experiment. EDTA buffer, 20 µl Proteinase K (20 mg ml–1; TaKaRa) Infection experiment. Intraperitoneal injection: and 10 µl 10% sodium dodecyl sulfate (SDS). After Ciliates collected from the 75 cm2 tissue-culture incubation at 55°C for 2 h, nucleic acids were extracted flasks were centrifuged at 500 × g for 10 min at room using TRIzol (Invitrogen) and chloroform. The eukary- temperature. One ml EMEM was added into the cell otic universal primers A (5’-ACC TGG TTG ATC CTG pellet and the resuspended ciliates were counted CCA GT-3’) (primer 1) and B (5’-TGA TCC TTC TGC using a haemocytometer. Twenty fish (8 to 10 g) in AGG TTC ACC TAC-3’) (primer 6), were used to each tank were each injected intraperitoneally with amplify the full-length eukaryotic SSU rDNA gene, fol- 50 µl of 1.0 to 1.4 × 104 or 106 cells fish–1 of YS1, WS1, lowed by thermal cycling with 40 amplification cycles YK1, JJ3, SCL-A, SCL-B and JK3 (Table 2).
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