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A New Species Myxodavisia Jejuensis N. Sp. (Myxosporea: Sinuolineidae) Isolated from Cultured Olive Flounder Paralichthys Olivaceus in South Korea

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A New Species Myxodavisia Jejuensis N. Sp. (Myxosporea: Sinuolineidae) Isolated from Cultured Olive Flounder Paralichthys Olivaceus in South Korea Parasitology Research (2019) 118:3105–3112 https://doi.org/10.1007/s00436-019-06454-z FISH PARASITOLOGY - ORIGINAL PAPER A new species Myxodavisia jejuensis n. sp. (Myxosporea: Sinuolineidae) isolated from cultured olive flounder Paralichthys olivaceus in South Korea Sang Phil Shin1 & Chang Nam Jin1 & Han Chang Sohn1 & Hiroshi Yokoyama2 & Jehee Lee1 Received: 10 April 2019 /Accepted: 4 September 2019/Published online: 14 September 2019 # Springer-Verlag GmbH Germany, part of Springer Nature 2019 Abstract A new myxosporean parasite, Myxodavisia jejuensis n. sp. (Myxozoa; Bivalvulida) is described from the urinary bladder of olive flounder Paralichthys olivaceus cultured on Jeju Island, Korea. Two long lateral appendages with whip-like extensions were attached to mature spores of triangular to semi-circular shape. The spores were measured at 13.1 ± 1.1 μm in length, 17.2 ± 1.0 μmin thickness, and 13.1 ± 1.0 μm in width. Two spherical polar capsules, with a diameter of 5.0 ± 0.4 μm, were observed on opposite sides in the middle of the spore. The suture line was straight or slightly sinuous on the middle of spores. The 18S rDNA from M. jejuensis n. sp. was used in BLAST and molecular phylogenetic analysis. The results demonstrated that M. jejuensis n. sp. was closest to Sinuolinea capsularis and that the infection site tropism was correlated with the phylogeny of marine myxosporeans. In addition, we designed specific primers to detect the 18S rDNA gene of M. jejuensis n. sp.; the results showed specific amplification in M. jejuensis n. sp. among the myxosporeans isolated from the urinary bladder of the cultured olive flounder. Keywords Myxodavisia jejuensis . Olive flounder . Infection site tropism . Polyphyly Introduction T. misguri;andthegenusHenneguya, including H. tridentigeri and Henneguya sp. were isolated from freshwater fish (Kim Over the past several decades, myxozoan parasites have been et al. 2002, 2013a, b;KimandKim2005; Cho et al. 2006a; studied globally, and over 2000 species have been reported to Choi et al. 2010;KwonandKim2011;Shinetal.2011;Seo date (Lom and Dykova 2006;Yangetal.2014). In Korea, et al. 2012;JeonandKim2015). In marine fish, Ceratomyxa various species of myxosporeans have been reported in fresh- protopsettae, C. oplegnathus, C. sparusaurati, Enteromyxum water and marine fishes since the first identification of leei, Kudoa paralichthys, K. iwatai, K. septempunctata, Thelohanellus kitauei in carp derived from Israel (Korean name: Parvicapsula anisocaudata, P. curv atura,andSphaerospora Hyang-eo or Israeli carp), Cyprinus carpio, in 1988 (Jun et al. koreana have been reported (Cho and Kim 2001, 2003, 2004, 1988). The genus Myxobolus, including M. miyairii, 2016; Cho et al. 2004, b; Song et al. 2013;Jeonetal.2017;Shin M. cheisini, M. koi, M. dispar, M. suturalis, M. episquamalis, et al. 2018b). In addition, parasites such as K. septempunctata and M. aeglefini; genus Thelohanellus, including T. kitauei and and E. leei cause food poisoning and economic loss (Kim et al. 2018;Shinetal.2018b). The genus Myxodavisia is a replacement name for Davisia; Section Editor: Astrid Holzer 28 Davisia spp. were transferred to a new genus Myxodavisia in 2008 (Zhao et al. 2008). These parasites mainly infect the * Jehee Lee urinary system of various fishes (M. amoena, M. anoplopoma, [email protected] M. aurita, M. bidens, M. brachiophora, M. cella, M. cornuta, 1 Department of Marine Life Science & Fish Vaccine Research Center, M. coryphaenoidia, M. diplocrepis, M. donecae, M. filiformis, Jeju National University, Jeju, Jeju Self-Governing Province 63243, M. galeiforme, M. hexagrammi, M. longibrachia, Republic of Korea M. longifilus, M. narvi, M. newfoundlandia, M. nototheniae, 2 Faculty of Veterinary Medicine, Okayama University of Science, M. opacita, M. ophidioni, M. pectoralis, M. reginae, Imabari, Ehime 794-8555, Japan M. sebastiscus, M. spectabilis,andM. spinosa), but some of 3106 Parasitol Res (2019) 118:3105–3112 them (M. bulani, M. cynoglossi, M. filiformis, M. haldarae, amplified by PCR using a combination of primers designed M. murtii,andM. sauridae) are isolated from the gall bladder by us (MyxodaF: 5′-ACTATGTTTAATACAGCTTGGTTG- (Zhao et al. 2008; Sarkar 2010; Fiala et al. 2015). To date, 3′ and MyxodaR: 5′-TCATTATTCAACTTGGTTCCC-3′) Myxodavisia spp. have not been reported in Korea and their and other groups (SSU_F04: 5′-GCTTGTCTCAAAGA pathogenicity is poorly understood. The Fish Vaccine TTAAGCC-3′, MYXGEN4f: 5′-GTGCCTTGAATAAA Research Center of Jeju National University has been moni- TCAGAG-3′,ACT1R:5′-AATTTCACCTCTCGCTGCCA- toring parasitic infections in cultured olive flounder 3′, and ERIB10: 5′-CTTCCGCAGGTTCACCTA-3′) (Barta Paralichthys olivaceus,starryflounderPlatichthys stellatus, et al. 1997; Hallett and Diamant 2001; Diamant et al. 2004; and rock bream Oplegnathus fasciatus. In our previous stud- Fonseca et al. 2010). PCR was conducted with the following ies, we have reported infections of E. leei, P. anisocaudata, cycling program: initial denaturation at 95 °C for 5 min and P. curvatura in olive flounder (Shin et al. 2018a, b). In the followed by 40 cycles at 95 °C for 30 s, 58 °C for 30 s, present study, we isolated a Myxodavisia species in the urinary 72 °C for 60 s, and a final extension at 72 °C for 10 min. bladder of cultured olive flounder. Morphological and phylo- PCR products were treated with AccuPrep Genomic PCR genetic analyses of the specimens suggested that this parasite Purification Kit (BIONEER, Korea) to remove excess primers represented a new species, which is described here as and dNTPs, and directly sequenced with BigDyeTM Myxodavisia jejuensis n. sp. Terminator v3.1 in an ABI 3730xl Sequencer. Multiple alignments of 18S rDNA sequence were performed by Clustal X 2.0 (Larkin et al. 2007) with the homologous Materials and methods sequences of Myxodavisia bulani available on the GenBank database, and the similarities of the present isolate and Parasite samples and partial purification M. bulani based on 18S rDNA were calculated in MEGA 7.0 (Kumar et al. 2016) and Clustal Omega (Sievers et al. 2011). Olive flounder samples (n = 18; total length, 26.0 ± 2.5 cm) Bayesian inference (BI) was used to reconstruct the phylogenet- were obtained dead from two olive flounder farms located ic tree from datasets containing 67 sequences of the 18S rDNA on Jeju island. Several fish exhibited urinary bladder enlarge- from the marine myxosporeans with the malacosporeans, name- ment. Extracts were aseptically obtained using a syringe and ly Tetracapsuloides bryosalmonae (KF731712), which was the urine suspensions were filtered through a 40-μmcell used as an outgroup. Ambiguously aligned regions in 18S strainer, followed by centrifugation at 10,000×g (3 min at rDNA datasets were removed using Gblocks v0.91b 20 °C). The pellets were resuspended in lysis buffer (RIPA, (Castresana 2000) under default parameters, allowing up to half Merck, Germany) for 5 min, and the suspensions were subse- the taxa to have gaps. For BI analysis, nucleotide substitution quently centrifuged at 10,000×g (1 min at 20 °C). The super- models were selected using the Akaike information criterion natant was discarded, and the pellet resuspended in phosphate (AIC) and the Bayesian information criterion (BIC), implement- buffered saline (PBS). The sample was collected and pre- ed in jModeltest 2.1.7 (Guindon and Gascuel 2003; Darriba served at 4 °C until further use. et al. 2012) and GTR + I + G was chosen as the best-fit nucle- otide substitution model for the 18S rDNA data sets. The metropolis-coupled Markov chain Monte Carlo (MCMC) algo- Morphological identification rithm implemented in MrBayes 3.2.4 (Ronquist et al. 2012)was run for a sufficient number of generations until the average The urine suspensions and partially purified parasites were standard deviation of the split frequencies was < 0.05. The sam- wet-mounted and observed under a light microscope and pling frequency was set at every 100 generations for 1000,000 photographed at 400 or × 1000 magnification. Myxospore generations. The first 100,000 generations from each run were measurements were taken from 20 spores using the image discarded as burn-in, and the remaining was analyzed using the processing program ImageJ, (available at http://rsb.info.nih. “sumt” command in MrBayes. Gaps were treated as missing gov/ij/) according to the criteria of Lom and Arthur (Lom data. A consensus tree was created using FigTree v1.4.2 and Arthur 1989). (http://tree.bio.ed.ac.uk/software/figtree/). Molecular identification and phylogenetic Diagnostic PCR for detecting M. jejuensis n. sp. analysis In order to detect M. jejuensis n. sp. in infected olive flounder, DNA was extracted from partially purified parasites using diagnostic PCR was carried out with the primers designed for QIAmp DNA Mini Kit (QIAGEN, Germany), following the this study. Each 20 μL reaction contained 0.2 μMMJdiaF(5′- manufacturer’s instructions. Portions of 18S rDNA were ACATTAAGCGAGAAACTATTGAAG-3′) and MJdiaR (5′- Parasitol Res (2019) 118:3105–3112 3107 CAACCAAGCTGTATTAAACATAGT-3′ ), 1 × filament with four to five turns, in a plane perpendicular to the EmeraldAmp PCR Master Mix (TaKaRa, Japan), and 1 μL sutural plane. The suture line straight or slightly sinous in the of sample DNA. Cycling conditions were initial denaturation middle of the spores. The sporoplasm fills spore cavity almost at 95 °C for 5 min, followed by 40 cycles at 95 °C for 30 s, or entirely with granular globules (Fig. 1b–e). Disporogonic 58 °C for 30 s, 72 °C for 30 s, and a final extension at 72 °C for plasmodia, with 25–28 μm in length, had two immature 7 min. To test the sensitivity and specificity of the developed spores with the posterior ends of both spores facing each other. diagnostic PCR, different dilutions of M. jejuensis n. sp. In addition, two mature spores with appendages, released myxospores and other myxosporeans infecting urinary blad- from the disporogonic plasmodia (Fig. 1f, g). der of olive flounder (such as P.
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